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.

Author Correction: The dental proteome of Homo antecessor.

An amendment to this paper has been published and can be accessed via a link at the top of the paper.

Inner morphological and metric characterization of the molar remains from the Montmaurin-La Niche mandible: The Neanderthal signal.

Here, we present a metric and morphological study of the molar remains from the Montmaurin-La Niche mandible by means of microcomputed tomography. According to the last analysis, based on the combination of geomorphological and paleontological data, the level bearing this human mandible probably corresponds to the marine isotope stages (MIS) 7. These data place the Montmaurin-La Niche in a chronologically intermediate position between the Neanderthals and the Middle Pleistocene fossils (e.g., Sima de los Huesos, la Caune de l'Arago). A recent study has revealed that while the mandible is more closely related to the Early and Middle Pleistocene African and Eurasian populations, the morphology of the outer enamel surfaces of its molars is typical of the Neanderthal linage. The data presented here are in line with this finding because the morphology of the enamel-dentine junction of the molars is similar to that of Neanderthals, whereas the absolute and relative enamel thickness values (2D and 3D) are closer to those exhibited by some Early Pleistocene hominins. Moreover, the pulp cavity morphology and proportions are in concordance with the Neanderthal populations. Our results strengthen the hypothesis that the settlement of Europe could be the result of several migrations, at different times, originated from a common source population. Thus, the variability in the European Middle Pleistocene populations (e.g., Montmaurin, Sima de los Huesos, Arago, Mala Balanica) could indicate different migrations at different times and/or population fragmentation, without excluding the possible hybridization between residents and new settlers.

First systematic assessment of dental growth and development in an archaic hominin (genus, Homo) from East Asia.

Several human dental traits typical of modern humans appear to be associated with the prolonged period of development that is a key human attribute. Understanding when, and in which early hominins, these dental traits first appeared is thus of strong interest. Using x-ray multiresolution synchrotron phase-contrast microtomography, we quantify dental growth and development in an archaic Homo juvenile from the Xujiayao site in northern China dating to 161,000-224,000 years or 104,000-125,000 years before present. Despite the archaic morphology of Xujiayao hominins, most aspects of dental development of this juvenile fall within modern human ranges (e.g., prolonged crown formation time and delayed first molar eruption). For its estimated age-at-death (6.5 years), its state of dental development is comparable to that of equivalently aged modern children. These findings suggest that several facets of modern human dental growth and development evolved in East Asia before the appearance of fully modern human morphology.

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.

Genome-wide patterns of selection in 230 ancient Eurasians.

Ancient DNA makes it possible to observe natural selection directly by analysing samples from populations before, during and after adaptation events. Here we report a genome-wide scan for selection using ancient DNA, capitalizing on the largest ancient DNA data set yet assembled: 230 West Eurasians who lived between 6500 and 300 bc, including 163 with newly reported data. The new samples include, to our knowledge, the first genome-wide ancient DNA from Anatolian Neolithic farmers, whose genetic material we obtained by extracting from petrous bones, and who we show were members of the population that was the source of Europe's first farmers. We also report a transect of the steppe region in Samara between 5600 and 300 bc, which allows us to identify admixture into the steppe from at least two external sources. We detect selection at loci associated with diet, pigmentation and immunity, and two independent episodes of selection on height.

The earliest unequivocally modern humans in southern China.

The hominin record from southern Asia for the early Late Pleistocene epoch is scarce. Well-dated and well-preserved fossils older than ∼45,000 years that can be unequivocally attributed to Homo sapiens are lacking. Here we present evidence from the newly excavated Fuyan Cave in Daoxian (southern China). This site has provided 47 human teeth dated to more than 80,000 years old, and with an inferred maximum age of 120,000 years. The morphological and metric assessment of this sample supports its unequivocal assignment to H. sapiens. The Daoxian sample is more derived than any other anatomically modern humans, resembling middle-to-late Late Pleistocene specimens and even contemporary humans. Our study shows that fully modern morphologies were present in southern China 30,000-70,000 years earlier than in the Levant and Europe. Our data fill a chronological and geographical gap that is relevant for understanding when H. sapiens first appeared in southern Asia. The Daoxian teeth also support the hypothesis that during the same period, southern China was inhabited by more derived populations than central and northern China. This evidence is important for the study of dispersal routes of modern humans. Finally, our results are relevant to exploring the reasons for the relatively late entry of H. sapiens into Europe. Some studies have investigated how the competition with H. sapiens may have caused Neanderthals' extinction (see ref. 8 and references therein). Notably, although fully modern humans were already present in southern China at least as early as ∼80,000 years ago, there is no evidence that they entered Europe before ∼45,000 years ago. This could indicate that H. neanderthalensis was indeed an additional ecological barrier for modern humans, who could only enter Europe when the demise of Neanderthals had already started.

Earliest evidence of pollution by heavy metals in archaeological sites.

Homo species were exposed to a new biogeochemical environment when they began to occupy caves. Here we report the first evidence of palaeopollution through geochemical analyses of heavy metals in four renowned archaeological caves of the Iberian Peninsula spanning the last million years of human evolution. Heavy metal contents reached high values due to natural (guano deposition) and anthropogenic factors (e.g. combustion) in restricted cave environments. The earliest anthropogenic pollution evidence is related to Neanderthal hearths from Gorham's Cave (Gibraltar), being one of the first milestones in the so-called "Anthropocene". According to its heavy metal concentration, these sediments meet the present-day standards of "contaminated soil". Together with the former, the Gibraltar Vanguard Cave, shows Zn and Cu pollution ubiquitous across highly anthropic levels pointing to these elements as potential proxies for human activities. Pb concentrations in Magdalenian and Bronze age levels at El Pirulejo site can be similarly interpreted. Despite these high pollution levels, the contaminated soils might not have posed a major threat to Homo populations. Altogether, the data presented here indicate a long-term exposure of Homo to these elements, via fires, fumes and their ashes, which could have played certain role in environmental-pollution tolerance, a hitherto neglected influence.

A mitochondrial genome sequence of a hominin from Sima de los Huesos.

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.

Facial morphogenesis of the earliest europeans.

The modern human face differs from that of our early ancestors in that the facial profile is relatively retracted (orthognathic). This change in facial profile is associated with a characteristic spatial distribution of bone deposition and resorption: growth remodeling. For humans, surface resorption commonly dominates on anteriorly-facing areas of the subnasal region of the maxilla and mandible during development. We mapped the distribution of facial growth remodeling activities on the 900-800 ky maxilla ATD6-69 assigned to H. antecessor, and on the 1.5 My cranium KNM-WT 15000, part of an associated skeleton assigned to African H. erectus. We show that, as in H. sapiens, H. antecessor shows bone resorption over most of the subnasal region. This pattern contrasts with that seen in KNM-WT 15000 where evidence of bone deposition, not resorption, was identified. KNM-WT 15000 is similar to Australopithecus and the extant African apes in this localized area of bone deposition. These new data point to diversity of patterns of facial growth in fossil Homo. The similarities in facial growth in H. antecessor and H. sapiens suggest that one key developmental change responsible for the characteristic facial morphology of modern humans can be traced back at least to H. antecessor.

Learning by heart: cultural patterns in the faunal processing sequence during the middle pleistocene.

Social learning, as an information acquisition process, enables intergenerational transmission and the stabilisation of cultural forms, generating and sustaining behavioural traditions within human groups. Archaeologically, such social processes might become observable by identifying repetitions in the record that result from the execution of standardised actions. From a zooarchaeological perspective, the processing and consumption of carcasses may be used to identify these types of phenomena at the sites. To investigate this idea, several faunal assemblages from Bolomor Cave (Valencia, Spain, MIS 9-5e) and Gran Dolina TD10-1 (Burgos, Spain, MIS 9) were analysed. The data show that some butchery activities exhibit variability as a result of multiple conditioning factors and, therefore, the identification of cultural patterns through the resulting cut-marks presents additional difficulties. However, other activities, such as marrow removal by means of intentional breakage, seem to reflect standardised actions unrelated to the physical characteristics of the bones. The statistical tests we applied show no correlation between the less dense areas of the bones and the location of impacts. Comparison of our experimental series with the archaeological samples indicates a counter-intuitive selection of the preferred locus of impact, especially marked in the case of Bolomor IV. This fact supports the view that bone breakage was executed counter-intuitively and repetitively on specific sections because it may have been part of an acquired behavioural repertoire. These reiterations differ between levels and sites, suggesting the possible existence of cultural identities or behavioural predispositions dependant on groups. On this basis, the study of patterns could significantly contribute to the identification of occupational strategies and organisation of the hominids in a territory. In this study, we use faunal data in identifying the mechanics of intergenerational information transmission within Middle Pleistocene human communities and provide new ideas for the investigation of occupational dynamics from a zooarchaeological approach.

Crown size and cusp proportions in Homo antecessor upper first molars. A comment on Quam et al. 2009.

A recent evaluation of upper first molar (M¹) crown size and cusp proportions in the genus Homo (Quam et al. 2009) describes Homo antecessor as maintaining a primitive pattern of cusp proportions, similar to that identified in australopithecines and the earliest members of the genus Homo. These results contrast with those of Gómez-Robles et al. (2007), who described the crown shape in these molars as derived and similar to Neanderthals and European Homo heidelbergensis. The reassessment of these measurements following the same methodology described by Quam et al. (2009) in all the M(1) s that are currently part of the hypodigm of H. antecessor demonstrates that the fossils from TD6 not only have the same cusp proportions identified in later Homo species, but also a strongly reduced metacone and a large hypocone shared with Middle and Upper Pleistocene members of the Neanderthal lineage. The evolutionary significance of these features should be evaluated in light of the results provided by recently discovered dental, cranial, mandibular, and postcranial H. antecessor fossils.