The rise and transformation of Bronze Age pastoralists in the Caucasus.

The Caucasus and surrounding areas, with their rich metal resources, became a crucible of the Bronze Age1 and the birthplace of the earliest steppe pastoralist societies2. Yet, despite this region having a large influence on the subsequent development of Europe and Asia, questions remain regarding its hunter-gatherer past and its formation of expansionist mobile steppe societies3-5. Here we present new genome-wide data for 131 individuals from 38 archaeological sites spanning 6,000 years. We find a strong genetic differentiation between populations north and south of the Caucasus mountains during the Mesolithic, with Eastern hunter-gatherer ancestry4,6 in the north, and a distinct Caucasus hunter-gatherer ancestry7 with increasing East Anatolian farmer admixture in the south. During the subsequent Eneolithic period, we observe the formation of the characteristic West Eurasian steppe ancestry and heightened interaction between the mountain and steppe regions, facilitated by technological developments of the Maykop cultural complex8. By contrast, the peak of pastoralist activities and territorial expansions during the Early and Middle Bronze Age is characterized by long-term genetic stability. The Late Bronze Age marks another period of gene flow from multiple distinct sources that coincides with a decline of steppe cultures, followed by a transformation and absorption of the steppe ancestry into highland populations.

Genome-wide population affinities and signatures of adaptation in hydruntines, sussemiones and Asian wild asses.

The extremely rich palaeontological record of the horse family, also known as equids, has provided many examples of macroevolutionary change over the last ~55 Mya. This family is also one of the most documented at the palaeogenomic level, with hundreds of ancient genomes sequenced. While these data have advanced understanding of the domestication history of horses and donkeys, the palaeogenomic record of other equids remains limited. In this study, we have generated genome-wide data for 25 ancient equid specimens spanning over 44 Ky and spread across Anatolia, the Caucasus, Central Asia and Mongolia. Our dataset includes the genomes from two extinct species, the European wild ass, Equus hydruntinus, and the sussemione Equus ovodovi. We document, for the first time, the presence of sussemiones in Mongolia and their survival around ~3.9 Kya, a finding that should be considered when discussing the timing of the first arrival of the domestic horse in the region. We also identify strong spatial differentiation within the historical ecological range of Asian wild asses, Equus hemionus, and incomplete reproductive isolation in several groups yet considered as different species. Finally, we find common selection signatures at ANTXR2 gene in European, Asian and African wild asses. This locus, which encodes a receptor for bacterial toxins, shows no selection signal in E. ovodovi, but a 5.4-kb deletion within intron 7. Whether such genetic modifications played any role in the sussemione extinction remains unknown.

Frontal sinuses and human evolution.

The frontal sinuses are cavities inside the frontal bone located at the junction between the face and the cranial vault and close to the brain. Despite a long history of study, understanding of their origin and variation through evolution is limited. This work compares most hominin species' holotypes and other key individuals with extant hominids. It provides a unique and valuable perspective of the variation in sinuses position, shape, and dimensions based on a simple and reproducible methodology. We also observed a covariation between the size and shape of the sinuses and the underlying frontal lobes in hominin species from at least the appearance of Homo erectus. Our results additionally undermine hypotheses stating that hominin frontal sinuses were directly affected by biomechanical constraints resulting from either chewing or adaptation to climate. Last, we demonstrate their substantial potential for discussions of the evolutionary relationships between hominin species.

Early Pleistocene stratigraphy, sedimentary environments, and formation contexts at Dmanisi in the Georgian Caucasus.

The Early Pleistocene site of Dmanisi is now well known for its large number of fossils of early Homo erectus as well as associated artifacts and faunal remains, recovered mainly in pipe-related geologic features. Testing in the M5 unit 100 m to the west of the main excavations revealed a thick stratigraphy with no evidence of pipes or gullies, indicating that the geologic record at Dmanisi included spatially distinct sedimentary environments that needed further investigation. Here we report the results of a geoarchaeological program to collect data bearing on contexts and formation processes over a large area of the promontory. That work has defined over 40,000 m2 of in situ deposits with artifacts and faunas. Stratum A ashes bury the uppermost Mashavera Basalt, which we have dated to 1.8 Ma in the M5 block. The Stratum A deposits contain stratified occupations that accumulated quickly and offer good potential for recovery of in situ materials. Stratum B1 deposits above the A/B unconformity include all of the pipe and gully facies at Dmanisi, reflecting a brief but very intense phase of geomorphic change. Those deposits contain the majority of faunas and all of the hominin fossils. B1 slope facies offer excellent formation contexts away from the piped area, and all B1 deposits are sealed by Stratum B2 over the whole promontory. Strata B2 to B5 register a return to slope facies, with no further evidence of pipes or gullies. Those deposits also present excellent contexts for recovery of in situ occupations. Overall, Dmanisi's geologic history preserves an exceptional record of the activities and environmental context of occupations during the first colonization of Eurasia.

Life and death at Dmanisi, Georgia: Taphonomic signals from the fossil mammals.

There are many hypotheses regarding influences on the early hominin biogeographic spread into Eurasia; among them is increased meat-eating. Dmanisi in Georgia is one of the rare Early Pleistocene sites in Eurasia, and here we present primary information and analysis of the medium and large mammal taphonomy, contributing information about site formation and the hominins' interaction with the fauna. Nearly 85% of the specimens come from the B1 stratum. Relative abundances of mammal families demonstrate some bias toward carnivores, especially Canis borjgali, and diverse Felidae species. Bones display little weathering. Post-depositional surface modifications and matrix obscure many bone surfaces, but carnivore tooth marking is the most common bone surface modification from the nutritive taphonomic phase. Tooth pits are large, in the size range of those made by modern Crocuta crocuta and Panthera leo. Breakage variables indicate most breaks occurred while the bones were still fresh, many by carnivore consumption. Fairly even limb bone representation of herbivores suggests carcasses were introduced to the site nearly whole. Hominin tool marks are present in low frequencies, but they suggest a variety of behaviors. These marks are found on Equus, Palaeotragus, Bison, large cervids, Pseudodama, Canis, and Mammuthus. Some were made by filleting proximal limb segments, and so are likely indicative of early access to carcasses, while other marks suggest scavenging. The Homo taphonomic variables resemble the rest of the taphonomic signatures from the site with little weathering, a slightly higher percentage of their bones are whole, but only a few have probable carnivore damage. The assemblage characteristics are compared to modern actualistic and experimental assemblages, and it is concluded that Dmanisi presents a palimpsest of hyena denning, felid activity, hominin meat-eating and likely natural deaths.

An ancient cranium from Dmanisi: Evidence for interpersonal violence, disease, and possible predation by carnivores on Early Pleistocene Homo.

Five well-preserved individuals from Dmanisi represent a paleodeme attributed to early Homo. Here we provide a case study of the D2280 adult cranium, which presents four oval-shaped lesions on the frontal, left parietal, and occipital bones. Several conditions are considered as possibly contributing to this pathology, including trauma, cysts, metastatic cancer, and infectious disease. One large but shallow depression on the left parietal bone has slightly elevated boundaries. Imaging reveals inner and outer tables that are reciprocally concave, so that the diploë is diminished or completely absent. This lesion is very likely a result of traumatic injury. Two additional depressions on the left side frontal and occipital bones may also be attributed to blunt force trauma. Such injuries stem from a variety of causes, but interpersonal violence may well be implicated. Based on the location and structure of a fourth lesion on the right-side frontal bone, we advance a possible diagnosis of treponemal disease. Lesions on the cranium and specifically on the frontal bone are common in treponemal disease. The condition develops as a periostitis, which eventually results in the destruction of the osteoperiosteal border of the cranial outer table and rarely involves the inner table. Additional perforations on the occipital bone are interpreted as perimortem damage resulting from predation by carnivores or scavenging by birds. If our reading of this cranial evidence can be confirmed, then D2280 documents one of the earliest instances of blunt force trauma in the Homo lineage. Dmanisi may also reveal the presence of treponemal disease in a population dated ca. 1.77 Ma ago. These findings bear on the social behavior of ancient humans and also the impact of infectious diseases on their survival.

A comparative study of the Early Pleistocene carnivore guild from Dmanisi (Georgia).

The carnivore guild of the Early Pleistocene site of Dmanisi is among the most diverse of the Early Pleistocene of the entire Old World. It includes 14 carnivoran taxa: Homotherium latidens, Megantereon whitei, Panthera onca georgica, Acinonyx pardinensis, Lynx issiodorensis; Pachycrocuta brevirostris; Canis (Xenocyon) lycaonoides, Canis borjgali, Vulpes alopecoides; Ursus etruscus; Lutra sp., Martes sp., Meles sp., and Pannonictis sp. The analysis of this rich carnivore guild was carried out under different methodological approaches to compare the assemblage with other chronological coeval European, Asian, and African sites from a paleobiological perspective. To achieve the goal, we used a permutational hierarchical method called boostrapping cluster analysis based on taxonomic absence/presence matrices (at both generic and specific level) and on ecological matrices (considering dietary preferences/hunting strategies of each carnivoran) and carried out Mantels tests assessing magnitude of time, space, ecology, and taxonomy as source of difference between guilds. Our results suggest a close similarity among the Dmanisi carnivore assemblage and other guilds recorded from European late Villafranchian sites such as Pirro Nord, Venta Micena, and Apollonia 1 and, in a lesser extent, to European Epivillafranchian sites as Vallonnet, Untermassfeld, or the Vallparadís Section. Early to Middle Pleistocene Asian carnivore assemblages display several similarities with the Dmanisi guild mainly in the record and diversity of felid and the canid ecomorphotypes. Eastern African sites such as Olduvai and Omo, as well as South African sites, display a lower similarity with the studied sample, basically for the most diverse hyenid taphocoenoses. To sum up, the present study suggests a close similarity between the Dmanisi carnivore guild and other European Late Early Pleistocene assemblages without close parallels with African or Asian assemblages.

Zoogeographic significance of Dmanisi large mammal assemblage.

We undertake a comparative mammalian zoogeographic analysis with the aim of revealing the extent to which the Dmanisi Early Pleistocene large mammal assemblage resembles, at the genus level, African, Arabian, and Eurasian localities of similar age. The inclusion of Old World Pliocene and Pleistocene mammalian faunas provides us with insights into the provincial origins of specific mammalian taxa and permits us to assess the relative affiliation of the Dmanisi mammalian faunas to other faunas in the Old World. Our analysis also allows us to consider hypotheses about the timing and direction of zoogeographic connections between western Eurasia and Africa during the Early Pleistocene. We utilize multiple zoogeographic analytical tools as a cross-comparison of Dmanisi with 42 other Eurasian and African mammalian-bearing localities between 2.7 and 0.7 Ma. Overall, we find that Dmanisi compares most closely with a subgroup of Greek, Italian, and Spanish localities that are slightly younger than Dmanisi itself. This could suggest a progressive dispersal from East to West of the large mammal communities during the late Early Pleistocene and the first occurrence at Dmanisi, and then later in Western Europe, of some taxa such as Stephanorhinus ex gr. etruscus-hundsheimensis, Equus altidens, Bison georgicus, Soergelia minor, Megantereon whitei, Canis borjgali, Canis (Xenocyon) lycaonoides. Dmanisi's habitats included drier areas, probably of open wooded savannah and grassland and by mountainous to semiarid rocky terrain. There is evidence that Dmanisi records short intervals of increased aridity in the middle part of the succession contemporaneous with the occurrence of Homo.

The Dmanisi Equus: Systematics, biogeography, and paleoecology.

The Equus datum has been established as a geochronologic 'instantaneous' migratory event of a North American Equus species into Eurasia at the beginning of the Pleistocene (2.58 Ma). A remarkable radiation of Equus followed across Eurasia and Africa. Dmanisi includes excellent remains of Equus, well calibrated between 1.85 and 1.76 Ma. Our morphologic and morphometric analyses of the augmented Dmanisi Equus sample support the co-occurrence of Equus stenonis and Equus altidens in the sequence. Dmanisi E. stenonis is found to be morphologically similar to the European E. stenonis populations and represents the best well-dated easternmost occurrence of this species in Eurasia. The Dmanisi E. altidens represents the oldest well-calibrated occurrence of this species in Western Eurasia. Our analyses demonstrate that E. altidens extended its range westward from west Asia to Greece, Germany, Italy, Spain, and possibly France. Our results do not support distinguishing multiple subspecies of E. altidens, including E. altidens altidens, E. altidens granatensis and E. stenonis mygdoniensis. The Dmanisi cranial and postcranial samples exhibit morphologies close both to extant hemiones and zebras. Equus altidens is believed to have been well adapted to newly emergent arid environments in western Eurasia during the late Early and early Middle Pleistocene. The first occurrence of E. altidens at Dmanisi marks an important turnover in the horse communities of the late Early Pleistocene, with a dispersion of this species from West Asia to West Europe ca. 1.8 Ma.

Genome-scale sequencing and analysis of human, wolf, and bison DNA from 25,000-year-old sediment.

Cave sediments have been shown to preserve ancient DNA but so far have not yielded the genome-scale information of skeletal remains. We retrieved and analyzed human and mammalian nuclear and mitochondrial environmental "shotgun" genomes from a single 25,000-year-old Upper Paleolithic sediment sample from Satsurblia cave, western Georgia:first, a human environmental genome with substantial basal Eurasian ancestry, which was an ancestral component of the majority of post-Ice Age people in the Near East, North Africa, and parts of Europe; second, a wolf environmental genome that is basal to extant Eurasian wolves and dogs and represents a previously unknown, likely extinct, Caucasian lineage; and third, a European bison environmental genome that is basal to present-day populations, suggesting that population structure has been substantially reshaped since the Last Glacial Maximum. Our results provide new insights into the Late Pleistocene genetic histories of these three species and demonstrate that direct shotgun sequencing of sediment DNA, without target enrichment methods, can yield genome-wide data informative of ancestry and phylogenetic relationships.

The early hunting dog from Dmanisi with comments on the social behaviour in Canidae and hominins.

The renowned site of Dmanisi in Georgia, southern Caucasus (ca. 1.8 Ma) yielded the earliest direct evidence of hominin presence out of Africa. In this paper, we report on the first record of a large-sized canid from this site, namely dentognathic remains, referable to a young adult individual that displays hypercarnivorous features (e.g., the reduction of the m1 metaconid and entoconid) that allow us to include these specimens in the hypodigm of the late Early Pleistocene species Canis (Xenocyon) lycaonoides. Much fossil evidence suggests that this species was a cooperative pack-hunter that, unlike other large-sized canids, was capable of social care toward kin and non-kin members of its group. This rather derived hypercarnivorous canid, which has an East Asian origin, shows one of its earliest records at Dmanisi in the Caucasus, at the gates of Europe. Interestingly, its dispersal from Asia to Europe and Africa followed a parallel route to that of hominins, but in the opposite direction. Hominins and hunting dogs, both recorded in Dmanisi at the beginning of their dispersal across the Old World, are the only two Early Pleistocene mammal species with proved altruistic behaviour towards their group members, an issue discussed over more than one century in evolutionary biology.

Paleoecology, biochronology, and paleobiogeography of Eurasian Rhinocerotidae during the Early Pleistocene: The contribution of the fossil material from Dmanisi (Georgia, Southern Caucasus).

Rhinocerotidae represents a common element in the Eurasian Pleistocene faunas. Origin, dispersal route, and biochronology of several species are still poorly understood due to gaps in the fossil record, in particular from central Eurasia. A remarkable collection of rhinoceros remains was recovered from the Early Pleistocene site of Dmanisi (Georgia). This collection is unique for the Early Pleistocene Rhinocerotidae records due to its abundance in remains, its age (ca 1.8 Ma) and geographic position (between Eastern and Western Eurasia). Two crania, which display some different morphological traits, are assigned to two different morphotypes and investigated by means of geometric morphometrics using landmarks and semilandmarks. Shapes in lateral and dorsal views of different Rhinocerotini species are compared with the studied crania to infer paleoecological information. The shape in the lateral view reflects ecological niche, in particular feeding type from browsing to grazing, and it also represent taxonomic discrimination. Morphotypes 1 and 2 from Dmanisi fall in two different clusters, corresponding to two different species, notably in lateral view. The results suggest a niche partitioning during the Early Pleistocene of Dmanisi between a browse-dominated and a grass-dominated mixed feeders, or possibly the presence of two ecomorphotypes of the same species. A comprehensive update of the Early Pleistocene occurrences of Eurasian Rhinocerotidae is reported in the discussion on the paleoecology of the extinct Northern Eurasian rhinocerotines.

The primitive brain of early Homo.

The brains of modern humans differ from those of great apes in size, shape, and cortical organization, notably in frontal lobe areas involved in complex cognitive tasks, such as social cognition, tool use, and language. When these differences arose during human evolution is a question of ongoing debate. Here, we show that the brains of early Homo from Africa and Western Asia (Dmanisi) retained a primitive, great ape-like organization of the frontal lobe. By contrast, African Homo younger than 1.5 million years ago, as well as all Southeast Asian Homo erectus, exhibited a more derived, humanlike brain organization. Frontal lobe reorganization, once considered a hallmark of earliest Homo in Africa, thus evolved comparatively late, and long after Homo first dispersed from Africa.

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.

Spatial patterning of the archaeological and paleontological assemblage at Dmanisi, Georgia: An analysis of site formation and carnivore-hominin interaction in Block 2.

This study addresses the roles of biotic agents in site formation in the B1 strata of Block 2 at Dmanisi, Georgia, using theoretical and analogous frameworks for the interpretation of spatial behaviors of carnivores and hominins. For this study, stone material, faunal remains, and coprolites are analyzed to determine if any spatially distinct behaviors can be identified, located, and attributed to either hominins or carnivores. Faunal, stone, and coprolite assemblages are compared with each other, and lithic, taxonomic, and taphonomic subassemblages are compared with the overall distribution of their parent material. The spatial and taphonomic signatures suggest that hominin activity was only a small part of the contributing factors to site formation, whereas carnivores played a major role in the accumulation of bone.

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.

The bears from Dmanisi and the first dispersal of early Homo out of Africa.

We report on the taxonomy and paleodiet of the bear population that inhabited the emblematic palaeoanthropological Early Pleistocene (1.8 Ma) site of Dmanisi (Georgia), based on a dual approach combining morphometrics and microwear of upper and lower teeth. Given that the teeth of Ursus etruscus Cuvier, 1823 from Dmanisi show considerable size variability, their systematic position has been debated. However, a comparative study of the coefficients of variation for tooth size measurements in several modern bear species shows that the variability in tooth size of the ursid population from Dmanisi could result from sexual dimorphism. The analysis of tooth microwear indicates that these bears inhabited a mixed environment of open plain with forest patches, where they had a browsing diet with a substantial contribution of meat and/or fish. Comparative tooth morphometric analyses of modern ursids and fossil U. etruscus indicate that this extinct species had an omnivorous behavior similar to that of extant brown bears. The ecological interactions of the Dmanisi bears with other members of the large mammals community, including the first hominins that dispersed out of Africa, are discussed in the light of this new evidence.

Early Pleistocene enamel proteome from Dmanisi resolves Stephanorhinus phylogeny.

The sequencing of ancient DNA has enabled the reconstruction of speciation, migration and admixture events for extinct taxa1. However, the irreversible post-mortem degradation2 of ancient DNA has so far limited its recovery-outside permafrost areas-to specimens that are not older than approximately 0.5 million years (Myr)3. By contrast, tandem mass spectrometry has enabled the sequencing of approximately 1.5-Myr-old collagen type I4, and suggested the presence of protein residues in fossils of the Cretaceous period5-although with limited phylogenetic use6. In the absence of molecular evidence, the speciation of several extinct species of the Early and Middle Pleistocene epoch remains contentious. Here we address the phylogenetic relationships of the Eurasian Rhinocerotidae of the Pleistocene epoch7-9, using the proteome of dental enamel from a Stephanorhinus tooth that is approximately 1.77-Myr old, recovered from the archaeological site of Dmanisi (South Caucasus, Georgia)10. Molecular phylogenetic analyses place this Stephanorhinus as a sister group to the clade formed by the woolly rhinoceros (Coelodonta antiquitatis) and Merck's rhinoceros (Stephanorhinus kirchbergensis). We show that Coelodonta evolved from an early Stephanorhinus lineage, and that this latter genus includes at least two distinct evolutionary lines. The genus Stephanorhinus is therefore currently paraphyletic, and its systematic revision is needed. We demonstrate that sequencing the proteome of Early Pleistocene dental enamel overcomes the limitations of phylogenetic inference based on ancient collagen or DNA. Our approach also provides additional information about the sex and taxonomic assignment of other specimens from Dmanisi. Our findings reveal that proteomic investigation of ancient dental enamel-which is the hardest tissue in vertebrates11, and is highly abundant in the fossil record-can push the reconstruction of molecular evolution further back into the Early Pleistocene epoch, beyond the currently known limits of ancient DNA preservation.