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Although a rich record of Pleistocene human-associated archaeological assemblages exists, the scarcity of hominin fossils often impedes the understanding of which hominins occupied a site. Using targeted enrichment of mitochondrial DNA, we show that cave sediments represent a rich source of ancient mammalian DNA that often includes traces of hominin DNA, even at sites and in layers where no hominin remains have been discovered. By automation-assisted screening of numerous sediment samples, we detected Neandertal DNA in eight archaeological layers from four caves in Eurasia. In Denisova Cave, we retrieved Denisovan DNA in a Middle Pleistocene layer near the bottom of the stratigraphy. Our work opens the possibility of detecting the presence of hominin groups at sites and in areas where no skeletal remains are found.

New human fossils from Jebel Irhoud (Morocco) document the earliest evolutionary stage of Homo sapiens and display modern conditions of the face and mandible combined with more primative features of the neurocranium. Early dawn for Homo sapiens The exact place and time that our species emerged remains obscure because the fossil record is limited and the chronological age of many key specimens remains uncertain. Previous fossil evidence has placed the emergence of modern human biology in eastern Africa around 200,000 years ago. In this issue of Nature , Jean-Jaques Hublin and colleagues report new human fossils from Jebel Irhoud, Morocco; their work is accompanied by a separate report on the dating of the fossils by Shannon McPherron and colleagues. Together they report remains dating back 300,000–350,000 years. They identify numerous features, including a facial, mandibular and dental morphology, that align the material with early or recent modern humans. They also identified more primitive neurocranial and endocranial morphology. Collectively, the researchers believe that this mosaic of features displayed by the Jebel Irhoud hominins assigns them to the earliest evolutionary phase of Homo sapiens . Both papers suggest that the evolutionary processes behind the emergence of modern humans were not confined to sub-Saharan Africa. Fossil evidence points to an African origin of Homo sapiens from a group called either H. heidelbergensis or H. rhodesiensis . However, the exact place and time of emergence of H. sapiens remain obscure because the fossil record is scarce and the chronological age of many key specimens remains uncertain. In particular, it is unclear whether the present day ‘modern’ morphology rapidly emerged approximately 200 thousand years ago (ka) among earlier representatives of H. sapiens 1 or evolved gradually over the last 400 thousand years 2 . Here we report newly discovered human fossils from Jebel Irhoud, Morocco, and interpret the affinities of the hominins from this site with other archaic and recent human groups. We identified a mosaic of features including facial, mandibular and dental morphology that aligns the Jebel Irhoud material with early or recent anatomically modern humans and more primitive neurocranial and endocranial morphology. In combination with an age of 315 ± 34 thousand years (as determined by thermoluminescence dating) 3 , this evidence makes Jebel Irhoud the oldest and richest African Middle Stone Age hominin site that documents early stages of the H. sapiens clade in which key features of modern morphology were established. Furthermore, it shows that the evolutionary processes behind the emergence of H. sapiens involved the whole African continent.

The oral microbiome plays key roles in human biology, health, and disease, but little is known about the global diversity, variation, or evolution of this microbial community. To better understand the evolution and changing ecology of the human oral microbiome, we analyzed 124 dental biofilm metagenomes from humans, including Neanderthals and Late Pleistocene to present-day modern humans, chimpanzees, and gorillas, as well as New World howler monkeys for comparison. We find that a core microbiome of primarily biofilm structural taxa has been maintained throughout African hominid evolution, and these microbial groups are also shared with howler monkeys, suggesting that they have been important oral members since before the catarrhine–platyrrhine split ca. 40 Mya. However, community structure and individual microbial phylogenies do not closely reflect host relationships, and the dental biofilms of Homo and chimpanzees are distinguished by major taxonomic and functional differences. Reconstructing oral metagenomes from up to 100 thousand years ago, we show that the microbial profiles of both Neanderthals and modern humans are highly similar, sharing functional adaptations in nutrient metabolism. These include an apparent Homo-specific acquisition of salivary amylase-binding capability by oral streptococci, suggesting microbial coadaptation with host diet. We additionally find evidence of shared genetic diversity in the oral bacteria of Neanderthal and Upper Paleolithic modern humans that is not observed in later modern human populations. Differences in the oral microbiomes of African hominids provide insights into human evolution, the ancestral state of the human microbiome, and a temporal framework for understanding microbial health and disease.

Denisovans are members of a hominin group who are currently only known directly from fragmentary fossils, the genomes of which have been studied from a single site, Denisova Cave 1 – 3 in Siberia. They are also known indirectly from their genetic legacy through gene flow into several low-altitude East Asian populations 4 , 5 and high-altitude modern Tibetans 6 . The lack of morphologically informative Denisovan fossils hinders our ability to connect geographically and temporally dispersed fossil hominins from Asia and to understand in a coherent manner their relation to recent Asian populations. This includes understanding the genetic adaptation of humans to the high-altitude Tibetan Plateau 7 , 8 , which was inherited from the Denisovans. Here we report a Denisovan mandible, identified by ancient protein analysis 9 , 10 , found on the Tibetan Plateau in Baishiya Karst Cave, Xiahe, Gansu, China. We determine the mandible to be at least 160 thousand years old through U-series dating of an adhering carbonate matrix. The Xiahe specimen provides direct evidence of the Denisovans outside the Altai Mountains and its analysis unique insights into Denisovan mandibular and dental morphology. Our results indicate that archaic hominins occupied the Tibetan Plateau in the Middle Pleistocene epoch and successfully adapted to high-altitude hypoxic environments long before the regional arrival of modern Homo sapiens . Fossil evidence indicates that Denisovans occupied the Tibetan Plateau in the Middle Pleistocene epoch and successfully adapted to this high-altitude hypoxic environments long before the regional arrival of modern Homo sapiens .

Nuclear DNA sequences from Middle Pleistocene Sima de los Huesos hominins show they were more closely related to Neanderthals than to Denisovans, and indicate a population divergence between Neanderthals and Denisovans that predates 430,000 years ago. Neanderthal-like hominins in Middle Pleistocene Spain This genomic analysis of Middle Pleistocene hominins from Sima de los Huesos in the Sierra de Atapuerca in Spain shows that they were more closely related to Neanderthals than to Denisovans, and indicates a divergence between Neanderthals and Denisovans that predates 430,000 years ago. A previous report based on analyses of mitochondrial genomes from these specimens had suggested close relationship to Denisovans, which was in contrast to other archaeological evidence including morphological features shared with Late Pleistocene Neanderthals. 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 1 . 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 2 . 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.

Homo naledi is a previously-unknown species of extinct hominin discovered within the Dinaledi Chamber of the Rising Star cave system, Cradle of Humankind, South Africa. This species is characterized by body mass and stature similar to small-bodied human populations but a small endocranial volume similar to australopiths. Cranial morphology of H. naledi is unique, but most similar to early Homo species including Homo erectus, Homo habilis or Homo rudolfensis. While primitive, the dentition is generally small and simple in occlusal morphology. H. naledi has humanlike manipulatory adaptations of the hand and wrist. It also exhibits a humanlike foot and lower limb. These humanlike aspects are contrasted in the postcrania with a more primitive or australopith-like trunk, shoulder, pelvis and proximal femur. Representing at least 15 individuals with most skeletal elements repeated multiple times, this is the largest assemblage of a single species of hominins yet discovered in Africa. Modern humans, or Homo sapiens, are now the only living species in their genus. But as recently as 100,000 years ago, there were several other species that belonged to the genus Homo. Together with modern humans, these extinct human species, our immediate ancestors and their close relatives, are collectively referred to as ‘hominins’. Now Berger et al. report the recent discovery of an extinct species from the genus Homo that was unearthed from deep underground in what has been named the Dinaledi Chamber, in the Rising Star cave system in South Africa. The species was named Homo naledi; ‘naledi’ means ‘star’ in Sotho (also called Sesotho), which is one of the languages spoken in South Africa. The unearthed fossils were from at least 15 individuals and include multiple examples of most of the bones in the skeleton. Based on this wide range of specimens from a single site, Berger et al. describe Homo naledi as being similar in size and weight to a small modern human, with human-like hands and feet. Furthermore, while the skull had several unique features, it had a small braincase that was most similar in size to other early hominin species that lived between four million and two million years ago. Homo naledi's ribcage, shoulders and pelvis also more closely resembled those of earlier hominin species than those of modern humans. The Homo naledi fossils are the largest collection of a single species of hominin that has been discovered in Africa so far and, in a related study, Dirks et al. describe the setting and context for these fossils. However, since the age of the fossils remains unclear, one of the next challenges will be to date the remains to provide more information about the early evolution of humans and their close relatives.

High-coverage sequencing of 79 (wild and captive) individuals representing all six non-human great ape species has identified over 88 million single nucleotide polymorphisms providing insight into ape genetic variation and evolutionary history and enabling comparison with human genetic diversity. Genetic picture of endangered great apes In an effort to provide insights into great ape genetic variation, the authors sequence 79 wild- and captive-born individuals from across all six great ape species and seven subspecies. Their data and analyses shed light on population structure and gene flow, inbreeding, inferred dynamics of effective population sizes and the differences in the rate of gene loss among the great apes. This new catalogue of great ape genome diversity provides a valuable resource for evolutionary and conservation studies. Most great ape genetic variation remains uncharacterized 1 , 2 ; however, its study is critical for understanding population history 3 , 4 , 5 , 6 , recombination 7 , selection 8 and susceptibility to disease 9 , 10 . Here we sequence to high coverage a total of 79 wild- and captive-born individuals representing all six great ape species and seven subspecies and report 88.8 million single nucleotide polymorphisms. Our analysis provides support for genetically distinct populations within each species, signals of gene flow, and the split of common chimpanzees into two distinct groups: Nigeria–Cameroon/western and central/eastern populations. We find extensive inbreeding in almost all wild populations, with eastern gorillas being the most extreme. Inferred effective population sizes have varied radically over time in different lineages and this appears to have a profound effect on the genetic diversity at, or close to, genes in almost all species. We discover and assign 1,982 loss-of-function variants throughout the human and great ape lineages, determining that the rate of gene loss has not been different in the human branch compared to other internal branches in the great ape phylogeny. This comprehensive catalogue of great ape genome diversity provides a framework for understanding evolution and a resource for more effective management of wild and captive great ape populations.

A full mitochondrial genome from a 400,000-year-old Middle Pleistocene hominin from Spain unexpectedly reveals a close relationship to Denisovans, a sister group to the Neanderthals, raising interesting questions about the origins of Neanderthals and Denisovans. Early hominin mtDNA from Atapuerca The human remains from the 'Sima de los Huesos' ('pit of bones') cave in Atapuerca, Spain, are of particular importance as they are from the poorly known Middle Pleistocene period, dating to more than 400,000 years ago. Now a near-complete genome sequence has been obtained from mitochondrial DNA (mtDNA) from a well-preserved femur from the collection, the oldest hominin genetic material so far recovered. Although Sima de los Huesos remains are often thought to represent a population close to the Neanderthal ancestry, the mtDNA suggests links with the still-enigmatic Denisovans of eastern Eurasia. It could be that the mtDNA is referring us to even earlier times, highlighting a common ancestor for Denisovans, Neanderthals and the Sima de los Huesos hominins, conventionally regarded as Homo heidelbergensis . 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 1 . One of these sites, the ‘Sima de los Huesos’ (‘pit of bones’), has yielded the world’s largest assemblage of Middle Pleistocene hominin fossils 2 , 3 , consisting of at least 28 individuals 4 dated to over 300,000 years ago 5 . The skeletal remains share a number of morphological features with fossils classified as Homo heidelbergensis and also display distinct Neanderthal-derived traits 6 , 7 , 8 . 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 9 , 10 , an eastern Eurasian sister group to Neanderthals. Our results pave the way for DNA research on hominins from the Middle Pleistocene.

Humans have a deep and innate sense of fairness. Humans, however, are not the only species to react to apparent inequities. Brosnan and de Waal propose that inequity aversion can be broken down into two levels. At the most basic level, individuals react to immediate unequal distribution of a reward for equal effort expended, whereas at the second, they show the ability to accept a current unequal distribution with the expectation that over time distribution will equalize. This second level facilitates cooperation over time and requires the cognitive abilities both to assess current distribution and envision future opportunities for equalization. As cognitive abilities advanced across the primate lineage, this more complex accounting of equal distribution and cooperation may have developed into the complete sense of fairness we see in humans today. Science , this issue 10.1126/science.1251776 The human sense of fairness is an evolutionary puzzle. To study this, we can look to other species, in which this can be translated empirically into responses to reward distribution. Passive and active protest against receiving less than a partner for the same task is widespread in species that cooperate outside kinship and mating bonds. There is less evidence that nonhuman species seek to equalize outcomes to their own detriment, yet the latter has been documented in our closest relatives, the apes. This reaction probably reflects an attempt to forestall partner dissatisfaction with obtained outcomes and its negative impact on future cooperation. We hypothesize that it is the evolution of this response that allowed the development of a complete sense of fairness in humans, which aims not at equality for its own sake but for the sake of continued cooperation.

Many ideas have been proposed to explain the origin of bipedalism in hominins and suspension in great apes (hominids); however, fossil evidence has been lacking. It has been suggested that bipedalism in hominins evolved from an ancestor that was a palmigrade quadruped (which would have moved similarly to living monkeys), or from a more suspensory quadruped (most similar to extant chimpanzees) 1 . Here we describe the fossil ape Danuvius guggenmosi (from the Allgäu region of Bavaria) for which complete limb bones are preserved, which provides evidence of a newly identified form of positional behaviour—extended limb clambering. The 11.62-million-year-old Danuvius is a great ape that is dentally most similar to Dryopithecus and other European late Miocene apes. With a broad thorax, long lumbar spine and extended hips and knees, as in bipeds, and elongated and fully extended forelimbs, as in all apes (hominoids), Danuvius combines the adaptations of bipeds and suspensory apes, and provides a model for the common ancestor of great apes and humans. Danuvius guggenmosi moved using extended limb clambering, thus combining adaptations of bipeds and suspensory apes and providing evidence of the evolution of bipedalism and suspension climbing in the common ancestor of great apes and humans.