Author Correction: The dental proteome of Homo antecessor.

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The dental proteome of Homo antecessor.

The phylogenetic relationships between hominins of the Early Pleistocene epoch in Eurasia, such as Homo antecessor, and hominins that appear later in the fossil record during the Middle Pleistocene epoch, such as Homo sapiens, are highly debated1-5. For the oldest remains, the molecular study of these relationships is hindered by the degradation of ancient DNA. However, recent research has demonstrated that the analysis of ancient proteins can address this challenge6-8. Here we present the dental enamel proteomes of H. antecessor from Atapuerca (Spain)9,10 and Homo erectus from Dmanisi (Georgia)1, two key fossil assemblages that have a central role in models of Pleistocene hominin morphology, dispersal and divergence. We provide evidence that H. antecessor is a close sister lineage to subsequent Middle and Late Pleistocene hominins, including modern humans, Neanderthals and Denisovans. This placement implies that the modern-like face of H. antecessor-that is, similar to that of modern humans-may have a considerably deep ancestry in the genus Homo, and that the cranial morphology of Neanderthals represents a derived form. By recovering AMELY-specific peptide sequences, we also conclude that the H. antecessor molar fragment from Atapuerca that we analysed belonged to a male individual. Finally, these H. antecessor and H. erectus fossils preserve evidence of enamel proteome phosphorylation and proteolytic digestion that occurred in vivo during tooth formation. Our results provide important insights into the evolutionary relationships between H. antecessor and other hominin groups, and pave the way for future studies using enamel proteomes to investigate hominin biology across the existence of the genus Homo.

Ectopic maxillary third molar in Early Pleistocene Homo antecessor from Atapuerca-Gran Dolina site (Burgos, Spain).

OBJECTIVES: Here we describe the case of an ectopic maxillary third molar (M3 ), preventing the eruption of the M2 , in the individual H3 of the hominin hypodigm of level TD6.2 of the Early Pleistocene site of Gran Dolina (Sierra de Atapuerca, Spain). MATERIALS AND METHODS: The fossil remains from the TD6.2 level of the Gran Dolina site (about 170 specimens) are assigned to Homo antecessor. Different geochronological methods place these hominins in the oxygen isotopic stage 21, between 0.8 and 0.85 million years ago (Ma). The immature individual H3 is represented by an almost complete midface (ATD6-69), preserving various teeth in situ. We used high-resolution microtomograhy (mCT) to investigate the abnormal position of the left M3 , virtually reconstruct M2 , and M3 as well as assessing the development stage of these. Finally, we compare this case with extinct and extant populations. RESULTS: Based on the identified signs, we suggest that individual H3 suffered from a unilateral impaction of the M2 as a result of the ectopic position of the developing M3 . DISCUSSION: We conclude that the most likely etiology for the ectopic position of the M3 is the lack of space in the maxilla. We discuss possible contributing factors, such as morphometric aspects of the maxilla and the early mineralization of the M3 , to support the M2 impaction. Finally, due to the early age at death of this individual we did not identify any secondary lesion associated with the M2 impaction.

Diet and environment 1.2 million years ago revealed through analysis of dental calculus from Europe's oldest hominin at Sima del Elefante, Spain.

Sima del Elefante, Atapuerca, Spain contains one of the earliest hominin fragments yet known in Europe, dating to 1.2 Ma. Dental calculus from a hominin molar was removed, degraded and analysed to recover entrapped remains. Evidence for plant use at this time is very limited and this study has revealed the earliest direct evidence for foods consumed in the genus Homo. This comprises starchy carbohydrates from two plants, including a species of grass from the Triticeae or Bromideae tribe, meat and plant fibres. All food was eaten raw, and there is no evidence for processing of the starch granules which are intact and undamaged. Additional biographical detail includes fragments of non-edible wood found adjacent to an interproximal groove suggesting oral hygiene activities, while plant fibres may be linked to raw material processing. Environmental evidence comprises spores, insect fragments and conifer pollen grains which are consistent with a forested environment.

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.

No known hominin species matches the expected dental morphology of the last common ancestor of Neanderthals and modern humans.

A central problem in paleoanthropology is the identity of the last common ancestor of Neanderthals and modern humans ([N-MH]LCA). Recently developed analytical techniques now allow this problem to be addressed using a probabilistic morphological framework. This study provides a quantitative reconstruction of the expected dental morphology of the [N-MH]LCA and an assessment of whether known fossil species are compatible with this ancestral position. We show that no known fossil species is a suitable candidate for being the [N-MH]LCA and that all late Early and Middle Pleistocene taxa from Europe have Neanderthal dental affinities, pointing to the existence of a European clade originated around 1 Ma. These results are incongruent with younger molecular divergence estimates and suggest at least one of the following must be true: (i) European fossils and the [N-MH]LCA selectively retained primitive dental traits; (ii) molecular estimates of the divergence between Neanderthals and modern humans are underestimated; or (iii) phenotypic divergence and speciation between both species were decoupled such that phenotypic differentiation, at least in dental morphology, predated speciation.

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 (

The first hominin of Europe.

The earliest hominin occupation of Europe is one of the most debated topics in palaeoanthropology. However, the purportedly oldest of the Early Pleistocene sites in Eurasia lack precise age control and contain stone tools rather than human fossil remains. Here we report the discovery of a human mandible associated with an assemblage of Mode 1 lithic tools and faunal remains bearing traces of hominin processing, in stratigraphic level TE9 at the site of the Sima del Elefante, Atapuerca, Spain. Level TE9 has been dated to the Early Pleistocene (approximately 1.2-1.1 Myr), based on a combination of palaeomagnetism, cosmogenic nuclides and biostratigraphy. The Sima del Elefante site thus emerges as the oldest, most accurately dated record of human occupation in Europe, to our knowledge. The study of the human mandible suggests that the first settlement of Western Europe could be related to an early demographic expansion out of Africa. The new evidence, with previous findings in other Atapuerca sites (level TD6 from Gran Dolina), also suggests that a speciation event occurred in this extreme area of the Eurasian continent during the Early Pleistocene, initiating the hominin lineage represented by the TE9 and TD6 hominins.

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. In this paper, we present new results obtained by combined Electron Spin Resonance/Uranium-series (ESR/U-series) dating on 20 herbivorous teeth from different levels at the Galería site. They are in agreement with the TL results for the upper part of the stratigraphic sequence (GIV and GIIIb), in the range of between 200 and 250 ka. But for the GIIIa to GIIb levels, the TL ages become abruptly older by 200 ka while ESR ages remain relatively constant. Finally, the TL and ESR data agree in the lowest part of the section (GIIa); both fall in the range of around 350-450 ka. Our results suggest a different interpretation for the GII, GIII and GIV units of Galería and the upper part of Gran Dolina (TD10 and TD11) than obtained by TL. The ESR/U-series results are supported by a Bayesian analysis, which allows a better integration between stratigraphic information and radiometric data.

New immature hominin fossil from European Lower Pleistocene shows the earliest evidence of a modern human dental development pattern.

Here we present data concerning the pattern of dental development derived from the microcomputed tomography (microCT) study of a recently discovered immature hominin mandible with a mixed dentition recovered from the TD6 level of the Gran Dolina Lower Pleistocene cave site in Sierra de Atapuerca, northern Spain. These data confirm our previous results that nearly 1 million years ago at least one European hominin species had a fully modern pattern of dental development with a clear slowdown in the development of the molar field regarding the anterior dental field. Furthermore, using available information about enamel formation times and root extension rates in chimpanzees, early hominins, and modern humans, we have estimated that the formation time of the upper and lower first molars of individual 5 (H5) from TD6, which had just erupted at the time of the death of this individual, ranges between 5.3 and 6.6 y. Therefore, the eruption time of the first permanent molars (M1) in the TD6 hominins was within the range of variation of modern human populations. Because the time of M1 eruption in primates is a robust marker of life history, we suggest, as a working hypothesis, that these hominins had a prolonged childhood in the range of the variation of modern humans. If this hypothesis is true, it implies that the appearance in Homo of this important developmental biological feature and an associated increase in brain size preceded the development of the neocortical areas leading to the cognitive capabilities that are thought to be exclusive to Homo sapiens.

Early Pleistocene human humeri from the Gran Dolina-TD6 site (Sierra de Atapuerca, Spain).

In this report, we present a morphometric comparative study of two Early Pleistocene humeri recovered from the TD6 level of the Gran Dolina cave site in Sierra de Atapuerca, northern Spain. ATD6-121 belongs to a child between 4 and 6 years old, whereas ATD6-148 corresponds to an adult. ATD6-148 exhibits the typical pattern of the genus Homo, but it also shows a large olecranon fossa and very thin medial and lateral pillars (also present in ATD6-121), sharing these features with European Middle Pleistocene hominins, Neandertals, and the Bodo Middle Pleistocene humerus. The morphology of the distal epiphysis, together with a few dental traits, suggests a phylogenetic relationship between the TD6 hominins and the Neandertal lineage. Given the older geochronological age of these hominins (ca. 900 ka), which is far from the age estimated by palaeogenetic studies for the population divergence of modern humans and Neandertals (ca. 400 ka), we suggest that this suite of derived "Neandertal" features appeared early in the evolution of the genus Homo. Thus, these features are not "Neandertal" apomorphies but traits which appeared in an ancestral and polymorphic population during the Early Pleistocene.

More than 500,000 years of right-handedness in Europe.

Considerable research supports the high frequency of right-handedness in living Homo sapiens, with worldwide rates of approximately nine right- for every one left-hander. Right-handedness appears to be a uniquely human trait, as no other primate species, no matter how proficient in tool use, shows frequencies even close to the strong right bias typical of humans (Cashmore, Uomini, & Chapelain, 2008; McGrew & Marchant 1997; Steele & Uomini, 2009). Here we review our research on human fossils from Sima de los Huesos (Atapuerca, Spain) and their likely descendants, the European Neandertals. We document hand preference in fossils by scratch patterns that occur on the labial (lip) face of incisors and canines, and contend that these patterns provide a reliable means for identifying predominant hand use in these samples. Manipulatory marks on the anterior teeth show a persistent pattern of right-handed actions, implying that the modern human pattern of dominant right-handedness extends deep into the European past.

Early Pleistocene human mandible from Sima del Elefante (TE) cave site in Sierra de Atapuerca (Spain): a comparative morphological study.

We present a detailed morphological comparative study of the hominin mandible ATE9-1 recovered in 2007 from the Sima del Elefante cave site in Sierra de Atapuerca, Burgos, northern Spain. Paleomagnetic analyses, biostratigraphical studies, and quantitative data obtained through nuclide cosmogenic methods, place this specimen in the Early Pleistocene (1.2-1.3 Ma). This finding, together with archaeological evidence from different European sites, suggests that Western Europe was colonised shortly after the first hominin expansion out of Africa around the Olduvai subchron. Our analysis of the ATE9-1 mandible includes a geometric morphometric analysis of the lower second premolar (LP(4)), a combined and detailed external and internal assessment of ATE9-1 roots through CT and microCT techniques, as well as a comparative study of mandibular and other dental features. This analysis reveals some primitive Homo traits on the external aspect of the symphysis and the dentition shared with early African Homo and the Dmanisi hominins. In contrast, other mandibular traits on the internal aspect of the symphysis are derived with regard to African early Homo, indicating unexpectedly large departures from patterns observed in Africa. Reaching the most occidental part of the Eurasian continent implies that the first African emigrants had to cross narrow corridors and to overcome geographic barriers favouring genetic drift, long isolation periods, and adaptation to new climatic and seasonal conditions. Given these conditions and that we are dealing with a long time period, it is possible that one or more speciation events could have occurred in this extreme part of Eurasia during the Early Pleistocene, originating in the lineages represented by the Sima del Elefante-TE9 hominins and possibly by the Gran Dolina-TD6 hominins. In the absence of any additional evidence, we prefer not include the specimen ATE9-1 in any named taxon and refer to it as Homo sp.

Early Pleistocene human mandible from Sima del Elefante (TE) cave site in Sierra de Atapuerca (Spain): a palaeopathological study.

Here we present a detailed palaeopathological study of the hominin mandible ATE9-1 found at the Sima del Elefante site (TE), Sierra de Atapuerca, Spain. This fossil represents the earliest hominin remains from Western Europe with an age of ca. 1.3 Ma. The specimen displays several dento-gnathic lesions; the antiquity and geographic location of this fossil justifies a detailed palaeopathological study to determine if the pathologies have significantly altered taxonomically relevant features. Our study reveals severe dental attrition combined with generalized hypercementosis, alveolar root exposure, mild periodontal disease, tooth dislocation, and an anomalous occlusal plane. We have also observed calculus deposits, two cystic lesions and an anomalous wear facet compatible with tooth picking. The majority of these pathological signs can be explained by compensatory eruption. We propose that these lesions are associated as causes, consequences, and amplifiers of one another within the framework of heavy and even traumatic occlusion, masticatory habits, or both traumatic occlusion and masticatory habits. Despite the severity of these lesions, occlusion was at least partially functional so it was unlikely to influence the survival of this individual. In addition, the lesions do not prohibit the taxonomic assessment of the mandible.

Unearthing Neanderthal population history using nuclear and mitochondrial DNA from cave sediments.

Bones and teeth are important sources of Pleistocene hominin DNA, but are rarely recovered at archaeological sites. Mitochondrial DNA (mtDNA) has been retrieved from cave sediments but provides limited value for studying population relationships. We therefore developed methods for the enrichment and analysis of nuclear DNA from sediments and applied them to cave deposits in western Europe and southern Siberia dated to between 200,000 and 50,000 years ago. We detected a population replacement in northern Spain about 100,000 years ago, which was accompanied by a turnover of mtDNA. We also identified two radiation events in Neanderthal history during the early part of the Late Pleistocene. Our work lays the ground for studying the population history of ancient hominins from trace amounts of nuclear DNA in sediments.

Short and long period growth markers of enamel formation distinguish European Pleistocene hominins.

Characterizing dental development in fossil hominins is important for distinguishing between them and for establishing where and when the slow overall growth and development of modern humans appeared. Dental development of australopiths and early Homo was faster than modern humans. The Atapuerca fossils (Spain) fill a barely known gap in human evolution, spanning ~1.2 to ~0.4 million years (Ma), during which H. sapiens and Neandertal dental growth characteristics may have developed. We report here perikymata counts, perikymata distributions and periodicities of all teeth belonging to the TE9 level of Sima del Elefante, level TD6.2 of Gran Dolina (H. antecessor) and Sima de los Huesos. We found some components of dental growth in the Atapuerca fossils resembled more recent H. sapiens. Mosaic evolution of perikymata counts and distribution generate three distinct clusters: H. antecessor, Sima de los Huesos and H. sapiens.

Neanderthal hunting strategies inferred from mortality profiles within the Abric Romaní sequence.

Ungulate mortality profiles are commonly used to study Neanderthal subsistence strategies. To assess the hunting strategies used by Neanderthals, we studied the ages at death of the cervids and equids found in levels E, H, I, Ja, Jb, K, L and M of the Abric Romaní sequence. These levels date between 43.2 ± 1.1 ka BP (14C AMS) and 54.5 ± 1.7 ka BP (U-series). The degree of eruption and development of the teeth and their wear stages were used to determine the ages of these animals at death, and mortality profiles were constructed using these data. The equids display prime dominated profiles in all of the analyzed levels, whereas the cervids display variable profiles. These results suggest that the Neanderthals of Abric Romaní employed both selective and non-selective hunting strategies. The selective strategy focused on the hunting of prime adults and generated prime dominated profiles. On the other hand, non-selective strategies, involved the consumption of animals of variable ages, resulting in catastrophic profiles. It is likely that in the selective hunting events were conducted using selective ambushes in which it was possible to select specific prey animals. On the other hand, encounter hunting or non-selective ambush hunting may have also been used at times, based on the abundances of prey animals and encounter rates. Specific hunting strategies would have been developed accordance with the taxa and the age of the individual to be hunted. The hunting groups most likely employed cooperative hunting techniques, especially in the capture of large animals. Thus, it is not possible to uniquely associate a single mortality profile with the predation tactics of Neanderthals at Abric Romaní.

The diet of the first Europeans from Atapuerca.

Hominin dietary specialization is crucial to understanding the evolutionary changes of craniofacial biomechanics and the interaction of food processing methods' effects on teeth. However, the diet-related dental wear processes of the earliest European hominins remain unknown because most of the academic attention has focused on Neandertals. Non-occlusal dental microwear provides direct evidence of the effect of chewed food particles on tooth enamel surfaces and reflects dietary signals over time. Here, we report for the first time the direct effect of dietary abrasiveness as evidenced by the buccal microwear patterns on the teeth of the Sima del Elefante-TE9 and Gran Dolina-TD6 Atapuerca hominins (1.2-0.8 million years ago - Myr) as compared with other Lower and Middle Pleistocene populations. A unique buccal microwear pattern that is found in Homo antecessor (0.96-0.8 Myr), a well-known cannibal species, indicates dietary practices that are consistent with the consumption of hard and brittle foods. Our findings confirm that the oldest European inhabitants ingested more mechanically-demanding diets than later populations because they were confronted with harsh, fluctuating environmental conditions. Furthermore, the influence of grit-laden food suggests that a high-quality meat diet from butchering processes could have fueled evolutionary changes in brain size.

Ontogeny of the maxilla in Neanderthals and their ancestors.

Neanderthals had large and projecting (prognathic) faces similar to those of their putative ancestors from Sima de los Huesos (SH) and different from the retracted modern human face. When such differences arose during development and the morphogenetic modifications involved are unknown. We show that maxillary growth remodelling (bone formation and resorption) of the Devil's Tower (Gibraltar 2) and La Quina 18 Neanderthals and four SH hominins, all sub-adults, show extensive bone deposition, whereas in modern humans extensive osteoclastic bone resorption is found in the same regions. This morphogenetic difference is evident by ∼5 years of age. Modern human faces are distinct from those of the Neanderthal and SH fossils in part because their postnatal growth processes differ markedly. The growth remodelling identified in these fossil hominins is shared with Australopithecus and early Homo but not with modern humans suggesting that the modern human face is developmentally derived.

New luminescence ages for the Galería Complex archaeological site: resolving chronological uncertainties on the acheulean record of the Sierra de Atapuerca, northern Spain.

The archaeological karstic infill site of Galería Complex, located within the Atapuerca system (Spain), has produced a large faunal and archaeological record (Homo sp. aff. heidelbergensis fossils and Mode II lithic artefacts) belonging to the Middle Pleistocene. Extended-range luminescence dating techniques, namely post-infrared infrared stimulated luminescence (pIR-IR) dating of K-feldspars and thermally transferred optically stimulated luminescence (TT-OSL) dating of individual quartz grains, were applied to fossil-bearing sediments at Galería. The luminescence dating results are in good agreement with published chronologies derived using alternative radiometric dating methods (i.e., ESR and U-series dating of bracketing speleothems and combined ESR/U-series dating of herbivore teeth), as well as biochronology and palaeoenvironmental reconstructions inferred from proxy records (e.g., pollen data). For the majority of samples dated, however, the new luminescence ages are significantly (∼50%) younger than previously published polymineral thermoluminescence (TL) chronologies, suggesting that the latter may have overestimated the true burial age of the Galería deposits. The luminescence ages obtained indicate that the top of the basal sterile sands (GIb) at Galería have an age of up to ∼370 thousand years (ka), while the lowermost sub-unit containing Mode II Acheulean lithics (base of unit GIIa) was deposited during MIS 9 (mean age = 313±14 ka; n = 4). The overlying units GIIb-GIV, which contain the richest archaeopalaeontological remains, were deposited during late MIS 8 or early MIS 7 (∼240 ka). Galería Complex may be correlative with other Middle Pleistocene sites from Atapuerca, such as Gran Dolina level TD10 and unit TE19 from Sima del Elefante, but the lowermost archaeological horizons are ∼100 ka younger than the hominin-bearing clay breccias at the Sima de los Huesos site. Our results suggest that both pIR-IR and single-grain TT-OSL dating are suitable for resolving Middle Pleistocene chronologies for the Sierra de Atapuerca karstic infill sequences.