Although an inverse relationship is expected in ancient DNA samples between the number of surviving DNA fragments and their length, ancient DNA sequencing libraries are strikingly deficient in ...molecules shorter than 40 bp. We find that a loss of short molecules can occur during DNA extraction and present an improved silica-based extraction protocol that enables their efficient retrieval. In combination with single-stranded DNA library preparation, this method enabled us to reconstruct the mitochondrial genome sequence from a Middle Pleistocene cave bear (Ursus deningeri) bone excavated at Sima de los Huesos in the Sierra de Atapuerca, Spain. Phylogenetic reconstructions indicate that the U. deningeri sequence forms an early diverging sister lineage to all Western European Late Pleistocene cave bears. Our results prove that authentic ancient DNA can be preserved for hundreds of thousand years outside of permafrost. Moreover, the techniques presented enable the retrieval of phylogenetically informative sequences from samples in which virtually all DNA is diminished to fragments shorter than 50 bp.
Some of the Sima de los Huesos (SH) humeri have been previously studied and described elsewhere. Here we present an updated inventory and a review of the specimens recovered to the present day. The ...morphological key traits of the adult and subadult specimens are described, discussed, and illustrated. The SH humeri share with Neandertals many traits usually considered to be Neandertal specializations, thus, most of this morphological pattern is not exclusive to them. The variation found within fossil samples stresses the frequential nature of all these traits and in the specific case of the SH humeri, most of the traits considered as phylogenetically relevant are retained by their descendants, the Neandertals. Some traits are plesiomorphic for the entire genus Homo or are present in European hominins since the early Pleistocene. Finally, some other traits display high variability within the SH sample or different hominin samples and are of uncertain phylogenetic value. Altogether, this evidence is consistent with the hypothesis based on the overall cranial and postcranial morphology that the SH hominins are a sister group to the later Neandertals.
The excellent fossil record from Sima de los Huesos (SH) includes three well‐known complete adult femora and several partial specimens that have not yet been published in detail. This fossil record ...provides an opportunity to analyze the morphology of European pre‐Neandertal adult femur and its variation with different evolution patterns. Currently, there are a minimum of five adult individuals (males or females). In this study, we compiled previously published basic anatomical and biometric characteristics of SH adult femora, emphasizing the most relevant features compared to other recent and fossil hominins. The SH femora exhibited a primitive morphological pattern common to all non‐Homo sapiens femora, as well as most of the Neandertal traits. Therefore, the complete Upper Pleistocene Neandertal pattern was well‐established in Middle Pleistocene ancestors long before the proper Neandertals appeared. Additionally, we highlight that the SH and Neandertal femora share some morphological traits and proportions with modern humans that hold sexual significance in our species, regardless of size. Keeping this in mind, we discussed the sex determination of the complete SH specimens and re‐evaluated sex allocation in two of them.
Current knowledge of the evolution of the postcranial skeleton in the genusHomois hampered by a geographically and chronologically scattered fossil record. Here we present a complete characterization ...of the postcranium of the middle Pleistocene paleodeme from the Sima de los Huesos (SH) and its paleobiological implications. The SH hominins show the following: (i) wide bodies, a plesiomorphic character in the genus Homo inherited fromtheir early hominin ancestors; (ii) statures that can be found in modern human middle-latitude populations that first appeared 1.6–1.5 Mya; and (iii) large femoral heads in some individuals, a trait that first appeared during the middle Pleistocene in Africa and Europe. The intrapopulational size variation in SH shows that the level of dimorphism was similar to modern humans (MH), but the SH hominins were less encephalized than Neandertals. SH shares many postcranial anatomical features with Neandertals. Although most of these features appear to be either plesiomorphic retentions or are of uncertain phylogenetic polarity, a few represent Neandertal apomorphies. Nevertheless, the full suite of Neandertal-derived features is not yet present in the SH population. The postcranial evidence is consistent with the hypothesis based on the cranial morphology that the SH hominins are a sister group to the later Neandertals. Comparison of the SH postcranial skeleton to other hominins suggests that the evolution of the postcranium occurred in a mosaic mode, both at a general and at a detailed level.
Recent chronological studies of the Sima de los Huesos (SH) hominin fossil site, Atapuerca, Spain, have established a close minimum age of at least 430 ka for sedimentary material immediately ...overlying the human remains. However, a firm maximum age limit still needs to be established for the SH fossils in order to better constrain the timing for the onset of Neandertal speciation. In the present study, we address this important chronological gap at SH by providing direct ages for the sediment deposits that host, and immediately underlie, the hominin fossils. Depositional ages were obtained using single-grain thermally-transferred optically stimulated luminescence (TT-OSL), a technique that has yielded reliable ‘extended-range’ luminescence chronologies at several independently dated Atapuerca sites. Four single-grain TT-OSL depositional ages of 453 ± 56 ka, 437 ± 38 ka, 457 ± 41 ka and 460 ± 39 ka were obtained for the red clay lithostratigraphic units (LU-5 and LU-6) found underlying and encasing the SH hominin bones. A Bayesian age-depth model was constructed using previously published chronologies, as well as the new single-grain TT-OSL ages for LU-5 and LU-6, in order to derive combined age estimates for individual lithostratigraphic units preserved at SH. The combined modeled ranges reveal that the hominin-bearing layer (LU-6) was deposited between 455 ± 17 ka and 440 ± 15 ka (mean lower and upper boundary 68.2% probability range ± 1σ uncertainty, respectively), with a mean age of 448 ± 15 ka. These new bracketing ages suggest that the hominin fossils at SH were most likely deposited within Marine Isotope Stage (MIS) 12, enabling more precise temporal constraint on the early evolution of the Neandertal lineage. The SH fossils represent the oldest reliably dated hominin remains displaying Neandertal features across Eurasia. These Neandertal features are first observed in the facial skeleton, including the mandible and teeth, as well as the temporomandibular joint, and appear consistently across the SH collection. Our chronological findings suggest that the appearance of these Neandertal traits may have been associated with the climatic demise of MIS 12 and the ecological changes that occurred in Iberia during this period. Other Middle Pleistocene hominin fossils from Europe dated to MIS 12–11, or later, show different morphological trends, with some lacking Neandertal specializations. The latest SH dating results enable improved temporal correlations with these contrasting hominin records from Europe, and suggest a complex picture for hominin evolution during the Middle Pleistocene.
Population genomic studies of ancient human remains have shown how modern-day European population structure has been shaped by a number of prehistoric migrations. The Neolithization of Europe has ...been associated with large-scale migrations from Anatolia, which was followed by migrations of herders from the Pontic steppe at the onset of the Bronze Age. Southwestern Europe was one of the last parts of the continent reached by these migrations, and modern-day populations from this region show intriguing similarities to the initial Neolithic migrants. Partly due to climatic conditions that are unfavorable for DNA preservation, regional studies on the Mediterranean remain challenging. Here, we present genome-wide sequence data from 13 individuals combined with stable isotope analysis from the north and south of Iberia covering a four-millennial temporal transect (7,500–3,500 BP). Early Iberian farmers and Early Central European farmers exhibit significant genetic differences, suggesting two independent fronts of the Neolithic expansion. The first Neolithic migrants that arrived in Iberia had low levels of genetic diversity, potentially reflecting a small number of individuals; this diversity gradually increased over time from mixing with local hunter-gatherers and potential population expansion. The impact of post-Neolithic migrations on Iberia was much smaller than for the rest of the continent, showing little external influence from the Neolithic to the Bronze Age. Paleodietary reconstruction shows that these populations have a remarkable degree of dietary homogeneity across space and time, suggesting a strong reliance on terrestrial food resources despite changing culture and genetic make-up.
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.
A unique assemblage of 28 hominin individuals, found in Sima de los Huesos in the Sierra de Atapuerca in Spain, has recently been dated to approximately 430,000 years ago. An interesting question is ...how these Middle Pleistocene hominins were related to those who lived in the Late Pleistocene epoch, in particular to Neanderthals in western Eurasia and to Denisovans, a sister group of Neanderthals so far known only from southern Siberia. While the Sima de los Huesos hominins share some derived morphological features with Neanderthals, the mitochondrial genome retrieved from one individual from Sima de los Huesos is more closely related to the mitochondrial DNA of Denisovans than to that of Neanderthals. However, since the mitochondrial DNA does not reveal the full picture of relationships among populations, we have investigated DNA preservation in several individuals found at Sima de los Huesos. Here we recover nuclear DNA sequences from two specimens, which show that the Sima de los Huesos hominins were related to Neanderthals rather than to Denisovans, indicating that the population divergence between Neanderthals and Denisovans predates 430,000 years ago. A mitochondrial DNA recovered from one of the specimens shares the previously described relationship to Denisovan mitochondrial DNAs, suggesting, among other possibilities, that the mitochondrial DNA gene pool of Neanderthals turned over later in their history.
Excavations of a complex of caves in the Sierra de Atapuerca in northern Spain have unearthed hominin fossils that range in age from the early Pleistocene to the Holocene. One of these sites, the ...'Sima de los Huesos' ('pit of bones'), has yielded the world's largest assemblage of Middle Pleistocene hominin fossils, consisting of at least 28 individuals dated to over 300,000 years ago. The skeletal remains share a number of morphological features with fossils classified as Homo heidelbergensis and also display distinct Neanderthal-derived traits. Here we determine an almost complete mitochondrial genome sequence of a hominin from Sima de los Huesos and show that it is closely related to the lineage leading to mitochondrial genomes of Denisovans, an eastern Eurasian sister group to Neanderthals. Our results pave the way for DNA research on hominins from the Middle Pleistocene.
Both animal hibernation and human renal osteodystrophy are characterized by high levels of serum parathyroid hormone. To test the hypothesis of hibernation in an extinct human species, we examined ...the hominin skeletal collection from Sima de los Huesos, Cave Mayor, Atapuerca, Spain, for evidence of hyperparathyroidism after a thorough review of the literature. We studied the morphology of the fossilized bones by using macrophotography, microscopy, histology and CT scanning. We found trabecular tunneling and osteitis fibrosa, subperiosteal resorption, ‘rotten fence post’ signs, brown tumours, subperiosteal new bone, chondrocalcinosis, rachitic osteoplaques and empty gaps between them, craniotabes, and beading of ribs mostly in the adolescent population of these hominins. Since many of the above lesions are pathognomonic, these extinct hominins suffered annually from renal rickets, secondary hyperparathyroidism, and renal osteodystrophy associated with Chronic Kidney Disease - Mineral and Bone Disorder (CKD-MBD). We suggest these diseases were caused by poorly tolerated hibernation in dark cavernous hibernacula. This is particularly evidenced by the rachitic osteoplaques and the gaps between them in some of the adolescent individuals along with the evidence of healing mainly in the adults. The sublayers in the rachitic osteoplaques indicate bouts of arousal from hibernation. The strong projection of the external lip of the femoral trochlea, the rachitic osteoplaques with the empty gaps between them, the “rotten fence post" sign, and the evidence of annual healing also point to the presence of annually intermittent puberty in this extinct human species. The hypothesis of hibernation is consistent with the genetic evidence and the fact that the SH hominins lived during an extreme glaciation. Alternative hypotheses are examined. The present work will provide a new insight into the physiological mechanism of early human metabolism which could help in determining the life histories and physiologies of extinct human species.
Les périodes d’hibernation chez l’animal et l’ostéodystrophie rénale en pathologie humaine sont associées à des taux sériques élevés d’hormone parathyroïdienne. Après une revue approfondie de la littérature, nous avons examiné la collection de squelettes d’hominidés de Sima de los Huesos, Cave Mayor, Atapuerca, Espagne, pour y rechercher des traces d’hypersécrétion parathyroïdienne. L’étude a été réalisée en associant macrophotographie, analyses microscopiques, histologiques et imagerie par tomodensitométrie. Nous avons observé principalement dans la population adolescente de ces homininés des aspects de tunnelisation osseuse trabéculaire, d’ostéite fibreuse, de résorption sous-périostée métaphysaire, de tumeurs brunes, d’ossification sous-périosté, de chondrocalcinose, des ostéophytes disséminés, de craniotabès et de perles costales. Plusieurs de ces lésions sont pathognomoniques et montrent que ces hominines étaient atteints chaque année d’ostéomalacie, d’hyperparathyroïdie secondaire et d’ostéodystrophie rénale. Nous estimons que ces troubles sont consécutifs à une hibernation dans des grottes sombres. Ceci est particulièrement mis en évidence par la présence de plaques osseuses rachitiques disséminées chez certains des adolescents, et de lésions cicatrisées principalement chez les adultes. Les sous-couches dans les plaques osseuses rachitiques indiquent des épisodes de suractivité liée à l’hibernation. La forte saillie de la lèvre externe de la trochlée fémorale, les plaques osseuses rachitiques séparées par des zones normales, les zones de résorption sous-périostée et les preuves de guérison annuelle indiquent également la présence d’une puberté intermittente chaque année chez cette espèce humaine disparue. Notre hypothèse rattachant ces lésions osseuses aux conséquences de l’hibernation est cohérente avec les arguments génétiques et le fait que les hominidés de SH ont vécu pendant une glaciation extrême. Des hypothèses alternatives sont examinées. Le présent travail apporte une approche novatrice des mécanismes physiologique du métabolisme des premiers humains qui pourrait aider à déterminer le cycle de vie et la physiologie des espèces humaines éteintes.
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