Life-history of Palaeoloxodon antiquus reveals Middle Pleistocene glacial refugium in the Megalopolis basin, Greece.

The Balkans are considered a major glacial refugium where flora and fauna survived glacial periods and repopulated the rest of Europe during interglacials. While it is also thought to have harboured Pleistocene human populations, evidence linking human activity, paleoenvironmental indicators and a secure temporal placement to glacial periods is scant. Here, we present the first intra-tooth multi-isotope analysis for the European straight-tusked elephant Palaeoloxodon antiquus, on an adult male individual excavated in association with lithic artefacts at the MIS 12 site Marathousa 1 (Megalopolis basin, Greece). The studied find also exhibits anthropogenic modifications, providing direct evidence of hominin presence. We employed strontium, carbon and oxygen isotope analysis on enamel bioapatite to investigate its foraging and mobility behaviour, using a sequential sampling strategy along the tooth growth axis of the third upper molar, to assess ecological changes during the last decade of life. We found a geographically restricted range, in a C3-dominated open woodland environment, and relatively stable conditions over the examined timeframe. Our results show that, despite the severity of the MIS 12 glacial, the Megalopolis basin sustained a mesic habitat, sufficient plant cover and limited seasonal fluctuations in resource availability, pointing to its role as a glacial refugium for both fauna and hominins.

Reconstructing patterns of domestication in reindeer using 3D muscle attachment areas.

The use of reindeer has been a crucial element in the subsistence strategies of past Arctic and Subarctic populations. However, the spatiotemporal occurrence of systematic herding practices has been difficult to identify in the bioarchaeological record. To address this research gap, this study proposes a new virtual anthropological approach for reconstructing habitual physical activity in reindeer, relying on the protocols of the "Validated Entheses based Reconstruction of Activity" (VERA) method. Following blind analytical procedures, we focused on eight muscle attachment sites ("entheses") in 36 reindeer free ranging in the wild, 21 specimens in captivity (zoo), and eight racing reindeer (habitual runners). Importantly, our analyses accounted for the effects of variation by subspecies, sex, age, and estimated body size. Our results showed clear differences across activity groups, leading to the development of discriminant function equations with cross-validated accuracies ranging from approximately 88 to 100%. The reliability of our functions was additionally confirmed using a blind test involving six zoo individuals not included in the initial dataset. Our findings support the use of the proposed approach for identifying domestication-related activities in zooarchaeological contexts, introducing a valuable tool for locating suspected domestication hotspots and elucidating the nature of past human-reindeer interactions. Supplementary Information: The online version contains supplementary material available at 10.1007/s12520-023-01910-5.

Inferring human neutral genetic variation from craniodental phenotypes.

There is a growing consensus that global patterns of modern human cranial and dental variation are shaped largely by neutral evolutionary processes, suggesting that craniodental features can be used as reliable proxies for inferring population structure and history in bioarchaeological, forensic, and paleoanthropological contexts. However, there is disagreement on whether certain types of data preserve a neutral signature to a greater degree than others. Here, we address this unresolved question and systematically test the relative neutrality of four standard metric and nonmetric craniodental data types employing an extensive computational genotype-phenotype comparison across modern populations from around the world. Our computation draws on the largest existing data sets currently available, while accounting for geographically structured environmental variation, population sampling uncertainty, disparate numbers of phenotypic variables, and stochastic variation inherent to a neutral model of evolution. Our results reveal that the four data types differentially capture neutral genomic variation, with highest signals preserved in dental nonmetric and cranial metric data, followed by cranial nonmetric and dental metric data. Importantly, we demonstrate that combining all four data types together maximizes the neutral genetic signal compared with using them separately, even with a limited number of phenotypic variables. We hypothesize that this reflects a lower level of genetic integration through pleiotropy between, compared to within, the four data types, effectively forming four different modules associated with relatively independent sets of loci. Therefore, we recommend that future craniodental investigations adopt holistic combined data approaches, allowing for more robust inferences about underlying neutral genetic variation.

Production method of the Königsaue birch tar documents cumulative culture in Neanderthals.

Birch tar is the oldest synthetic substance made by early humans. The earliest such artefacts are associated with Neanderthals. According to traditional interpretations, their study allows understanding Neanderthal tool behaviours, skills and cultural evolution. However, recent work has found that birch tar can also be produced with simple processes, or even result from fortuitous accidents. Even though these findings suggest that birch tar per se is not a proxy for cognition, they do not shed light on the process by which Neanderthals produced it, and, therefore, cannot evaluate the implications of that behaviour. Here, we address the question of how tar was made by Neanderthals. Through a comparative chemical analysis of the two exceptional birch tar pieces from Königsaue (Germany) and a large reference birch tar collection made with Stone Age techniques, we found that Neanderthals did not use the simplest method to make tar. Rather, they distilled tar in an intentionally created underground environment that restricted oxygen flow and remained invisible during the process. This degree of complexity is unlikely to have been invented spontaneously. Our results suggest that Neanderthals invented or developed this process based on previous simpler methods and constitute one of the clearest indicators of cumulative cultural evolution in the European Middle Palaeolithic. Supplementary information: The online version contains supplementary material available at 10.1007/s12520-023-01789-2.

Icex: Advances in the automatic extraction and volume calculation of cranial cavities.

The use of non-destructive approaches for digital acquisition (e.g. computerised tomography-CT) allows detailed qualitative and quantitative study of internal structures of skeletal material. Here, we present a new R-based software tool, Icex, applicable to the study of the sizes and shapes of skeletal cavities and fossae in 3D digital images. Traditional methods of volume extraction involve the manual labelling (i.e. segmentation) of the areas of interest on each section of the image stack. This is time-consuming, error-prone and challenging to apply to complex cavities. Icex facilitates rapid quantification of such structures. We describe and detail its application to the isolation and calculation of volumes of various cranial cavities. The R tool is used here to automatically extract the orbital volumes, the paranasal sinuses, the nasal cavity and the upper oral volumes, based on the coordinates of 18 cranial anatomical points used to define their limits, from 3D cranial surface meshes obtained by segmenting CT scans. Icex includes an algorithm (Icv) for the calculation of volumes by defining a 3D convex hull of the extracted cavity. We demonstrate the use of Icex on an ontogenetic sample (0-19 years) of modern humans and on the fossil hominin crania Kabwe (Broken Hill) 1, Gibraltar (Forbes' Quarry) and Guattari 1. We also test the tool on three species of non-human primates. In the modern human subsample, Icex allowed us to perform a preliminary analysis on the absolute and relative expansion of cranial sinuses and pneumatisations during growth. The performance of Icex, applied to diverse crania, shows the potential for an extensive evaluation of the developmental and/or evolutionary significance of hollow cranial structures. Furthermore, being open source, Icex is a fully customisable tool, easily applicable to other taxa and skeletal regions.

Evolution of Homo in the Middle and Late Pleistocene.

The Middle and Late Pleistocene is arguably the most interesting period in human evolution. This broad period witnessed the evolution of our own lineage, as well as that of our sister taxon, the Neanderthals, and related Denisovans. It is exceptionally rich in both fossil and archaeological remains, and uniquely benefits from insights gained through molecular approaches, such as paleogenetics and paleoproteomics, that are currently not widely applicable in earlier contexts. This wealth of information paints a highly complex picture, often described as 'the Muddle in the Middle,' defying the common adage that 'more evidence is needed' to resolve it. Here we review competing phylogenetic scenarios and the historical and theoretical developments that shaped our approaches to the fossil record, as well as some of the many remaining open questions associated with this period. We propose that advancing our understanding of this critical time requires more than the addition of data and will necessitate a major shift in our conceptual and theoretical framework.

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.

The Application of Bony Labyrinth Methods for Forensic Affinity Estimation.

Population affinity identification is important for reconstructing the biological profile of human skeletal remains. Most anthropological methods for predicting population affinity rely on complete crania or cranial parts. However, complete parts are frequently not found in forensic and bioarchaeological contexts. In contrast, the petrous portion of the cranium presents a unique rate of preservation in the field. Therefore, this study aimed to develop stepwise discriminant function formulae to determine population affinity using measurements on three-dimensional models of the human adult bony labyrinth. The sample utilised consisted of 30 German, 38 African Zulu, and 30 Oneota individuals. A total of four function equations were developed. The function involving all three populations presented an average accuracy of 90.8%. Mathematical equations were also derived to discriminate between Zulu and Germans (91.2%), Zulu and Oneota (95.5%), as well as Oneota and Germans (96.7%). These results indicate this new method of population affinity identification is highly successful, even with fragmentary remains.

First record of Macaca (Cercopithecidae, Primates) in the Middle Pleistocene of Greece.

In this article, we describe an almost complete macaque mandible from the Middle Pleistocene locality Marathousa 1 in the Megalopolis Basin of southern Greece. The mandible belonged to a male individual of advanced ontogenetic age and of estimated body mass ∼13 kg. Comparative metric analysis of its teeth permits its attribution to the Barbary macaque Macaca sylvanus, a species that was geographically widely distributed in Western Eurasia during the Plio-Pleistocene. The dental dimensions of the Marathousa 1 macaque fit better within the variation of the Early Pleistocene M. s. florentina and the Middle to Late Pleistocene M. s. pliocena rather than with the extant representative M. s. sylvanus. Moreover, principal component analysis reveals a better match with M. s. pliocena. However, because no clear-cut diagnostic criteria have been defined to differentiate these European fossil subspecies, we attribute the Marathousa 1 specimen to M. s. cf. pliocena, in agreement with the chronology of the locality. Previously known only from the Early Pleistocene of Greece by some isolated teeth, this is the first record of Macaca in the Middle Pleistocene of the country and one of very few in the eastern sector of the peri-Mediterranean region. We discuss the presence of macaques in the paleolake environment of Marathousa 1, as well as their predation risks from both carnivores and hominins present at the locality.

3D geometric morphometrics analysis of mandibular fragments of Ouranopithecus macedoniensis from the late Miocene deposits of Central Macedonia, Greece.

OBJECTIVES: To explore mandibular shape differences between Ouranopithecus macedoniensis and a comparative sample of extant great apes using three-dimensional (3D) geometrics morphometrics. Other objectives are to assess mandibular shape variation and homogeneity within Ouranopithecus, explore the effects of size on mandibular shape, and explore the degree of mandibular sexual size dimorphism in Ouranopithecus. MATERIALS AND METHODS: The comparative sample comprises digitized mandibles from adult extant great apes. The 3D analysis includes three datasets: one with landmarks registered on the mandibular corpus and symphysis of mandibles preserving both sides, one on hemimandibles only, and one focused on the ramus and gonial area. Multivariate statistical analyses were conducted, such as ordination analyses (PCA), intra-specific Procrustes distances pairs, pairwise male-female centroid size differences, and correlation analyses. RESULTS: The male and female specimens of Ouranopithecus have mandibular shapes that are quite similar, although differences exist. The Procrustes distances results suggest more shape variation in Ouranopithecus than in the extant great apes. Ouranopithecus shows some similarities in mandibular shape to the larger great apes, Gorilla and Pongo. Moreover, the degree of sexual dimorphism in the small Ouranopithecus sample is greater than any of the great apes. Based on our correlation analyses of principal components (PC) with size, some PCs are significantly correlated with size, with correlation varying from moderate to substantial. DISCUSSION: This study attempted to understand better the variation within the mandibles of O. macedoniensis and the expression of sexual dimorphism in this taxon in more detail than has been done previously. The overall mandibular morphology of Ouranopithecus shows some similarities to those of the larger great apes, which likely reflects similarities in size. Compared to Gorilla and Pongo, O. macedoniensis shows an elevated degree of morphological variation, although limitations relating to sample size apply. Sexual dimorphism in the mandibles of O. macedoniensis appears to be relatively high, seemingly greater than in Gorilla and high even in comparison to Pongo, but this again is possibly in part an artifact of a small sample size.

Archaeometric evidence for the earliest exploitation of lignite from the bronze age Eastern Mediterranean.

This paper presents the earliest evidence for the exploitation of lignite (brown coal) in Europe and sheds new light on the use of combustion fuel sources in the 2nd millennium BCE Eastern Mediterranean. We applied Thermal Desorption/Pyrolysis-Gas Chromatography-Mass Spectrometry and Polarizing Microscopy to the dental calculus of 67 individuals and we identified clear evidence for combustion markers embedded within this calculus. In contrast to the scant evidence for combustion markers within the calculus samples from Egypt, all other individuals show the inhalation of smoke from fires burning wood identified as Pinaceae, in addition to hardwood, such as oak and olive, and/or dung. Importantly, individuals from the Palatial Period at the Mycenaean citadel of Tiryns and the Cretan harbour site of Chania also show the inhalation of fire-smoke from lignite, consistent with the chemical signature of sources in the northwestern Peloponnese and Western Crete respectively. This first evidence for lignite exploitation was likely connected to and at the same time enabled Late Bronze Age Aegean metal and pottery production, significantly by both male and female individuals.

Accurate and semi-automated reassociation of intermixed human skeletal remains recovered from bioarchaeological and forensic contexts.

Commingled remains describes the situation of intermixed skeletal elements, an extremely common occurrence in contemporary forensic cases, archaeological mass graves, as well as fossil hominin assemblages. Given that reliable identification is typically impossible for commingled contexts, a plethora of previous studies has focused on the development of refined methods for reassociating the bones of each individual skeleton. Here, a novel virtual approach for quantifying the degree of three-dimensional shape compatibility between two adjoining bone articular surfaces is put forth. Additionally, the integrability of this method with traditional osteometric techniques is evaluated. We focus on the paradigm of the hip joint, whose articulating bone elements (the femur and the innominate bone) are crucial for reconstructing the biological profile of unidentified human remains. The results demonstrate that this new semi-automated methodology is highly accurate both for large commingled assemblages (such as those resulting from mass disasters or burials) as well as smaller-scale contexts (such as those resulting from secondary burials).

Katerina Harvati.

Interview with paleoanthropologist Katerina Harvati, who studies Neanderthal evolution and modern human origins at the Eberhard Karls University of Tübingen.

The evolution and changing ecology of the African hominid oral microbiome.

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.

New horizons in reconstructing past human behavior: Introducing the "Tübingen University Validated Entheses-based Reconstruction of Activity" method.

An accurate reconstruction of habitual activities in past populations and extinct hominin species is a paramount goal of paleoanthropological research, as it can elucidate the evolution of human behavior and the relationship between culture and biology. Variation in muscle attachment (entheseal) morphology has been considered an indicator of habitual activity, and many attempts have been made to use it for this purpose. However, its interpretation remains equivocal due to methodological shortcomings and a paucity of supportive experimental data. Through a series of studies, we have introduced a novel and precise methodology that focuses on reconstructing muscle synergies based on three-dimensional and multivariate analyses among entheses. This approach was validated using uniquely documented anthropological samples, experimental animal studies, histological observations, and geometric morphometrics. Here, we detail, synthesize, and critically discuss the findings of these studies, which overall point to the great potential of entheses in elucidating aspects of past human behavior.

Biomechanics of the human thumb and the evolution of dexterity.

Systematic tool production and use is one of humanity's defining characteristics, possibly originating as early as >3 million years ago.1-3 Although heightened manual dexterity is considered to be intrinsically intertwined with tool use and manufacture, and critical for human evolution, its role in the emergence of early culture remains unclear. Most previous research on this question exclusively relied on direct morphological comparisons between early hominin and modern human skeletal elements, assuming that the degree of a species' dexterity depends on its similarity with the modern human form. Here, we develop a new approach to investigate the efficiency of thumb opposition, a fundamental component of manual dexterity, in several species of fossil hominins. Our work for the first time takes into account soft tissue as well as bone anatomy, integrating virtual modeling of musculus opponens pollicis and its interaction with three-dimensional bone shape form. Results indicate that a fundamental aspect of efficient thumb opposition appeared approximately 2 million years ago, possibly associated with our own genus Homo, and did not characterize Australopithecus, the earliest proposed stone tool maker. This was true also of the late Australopithecus species, Australopithecus sediba, previously found to exhibit human-like thumb proportions. In contrast, later Homo species, including the small-brained Homo naledi, show high levels of thumb opposition dexterity, highlighting the increasing importance of cultural processes and manual dexterity in later human evolution.

Prevalence of cranial trauma in Eurasian Upper Paleolithic humans.

OBJECTIVES: This study characterizes patterns of cranial trauma prevalence in a large sample of Upper Paleolithic (UP) fossil specimens (40,000-10,000 BP). MATERIALS AND METHODS: Our sample comprised 234 individual crania (specimens), representing 1,285 cranial bones (skeletal elements), from 101 Eurasian UP sites. We used generalized linear mixed models (GLMMs) to assess trauma prevalence in relation to age-at-death, sex, anatomical distribution, and between pre- and post-Last Glacial Maximum (LGM) samples, while accounting for skeletal preservation. RESULTS: Models predicted a mean cranial trauma prevalence of 0.07 (95% CI 0.003-0.19) at the level of skeletal elements, and of 0.26 (95% CI 0.08-0.48) at the level of specimens, each when 76-100% complete. Trauma prevalence increased with skeletal preservation. Across specimen and skeletal element datasets, trauma prevalence tended to be higher for males, and was consistently higher in the old age group. We found no time-specific trauma prevalence patterns for the two sexes or age cohorts when comparing samples from before and after the LGM. Samples showed higher trauma prevalence in the vault than in the face, with vault remains being affected predominantly in males. DISCUSSION: Cranial trauma prevalence in UP humans falls within the variation described for Mesolithic and Neolithic samples. According to our current dataset, UP males and females were exposed to slightly different injury risks and trauma distributions, potentially due to different activities or behaviors, yet both sexes exhibit more trauma among the old. Environmental stressors associated with climatic changes of the LGM are not reflected in cranial trauma prevalence. To analyze trauma in incomplete skeletal remains we propose GLMMs as an informative alternative to crude frequency calculations.

Biocultural evidence of precise manual activities in an Early Holocene individual of the high-altitude Peruvian Andes.

OBJECTIVES: Cuncaicha, a rockshelter site in the southern Peruvian Andes, has yielded archaeological evidence for human occupation at high elevation (4,480 masl) during the Terminal Pleistocene (12,500-11,200 cal BP), Early Holocene (9,500-9,000 cal BP), and later periods. One of the excavated human burials (Feature 15-06), corresponding to a middle-aged female dated to ~8,500 cal BP, exhibits skeletal osteoarthritic lesions previously proposed to reflect habitual loading and specialized crafting labor. Three small tools found in association with this burial are hypothesized to be associated with precise manual dexterity. MATERIALS AND METHODS: Here, we tested this functional hypothesis through the application of a novel multivariate methodology for the three-dimensional analysis of muscle attachment surfaces (entheses). This original approach has been recently validated on both lifelong-documented anthropological samples as well as experimental studies in nonhuman laboratory samples. Additionally, we analyzed the three-dimensional entheseal shape and resulting moment arms for muscle opponens pollicis. RESULTS: Results show that Cuncaicha individual 15-06 shows a distinctive entheseal pattern associated with habitual precision grasping via thumb-index finger coordination, which is shared exclusively with documented long-term precision workers from recent historical collections. The separate geometric morphometric analysis revealed that the individual's opponens pollicis enthesis presents a highly projecting morphology, which was found to strongly correlate with long joint moment arms (a fundamental component of force-producing capacity), closely resembling the form of Paleolithic hunter-gatherers from diverse geo-chronological contexts of Eurasia and North Africa. DISCUSSION: Overall, our findings provide the first biocultural evidence to confirm that the lifestyle of some of the earliest Andean inhabitants relied on habitual and forceful precision grasping tasks.

Frontal bone virtual reconstruction and geometric morphometric analysis of the mid-Pleistocene hominin KNM-OG 45500 (Olorgesailie, Kenya).

KNM-OG 45500 is a hominin fossil composed of parts of a frontal bone, left temporal bone, and cranial vault pieces. Since its discovery along the Olorgesailie Formation (Kenya) in 2003, it has been associated with the Homo erectus hypodigm. The specimen, derived from a geological context dated to ca. 900 Ka BP, has been described as a very small individual of probable female sex. However, despite its status as an important hominin specimen, it has not been used in a quantitative comparative framework because of its fragmentary condition. Here, we undertake a virtual reconstruction of the better-preserved fragment, the frontal bone. We additionally apply geometric morphometric analyses, using a geographically diverse fossil and modern human sample, in order to investigate the morphological affinities of KNM-OG 45500. Our results show that the frontal shape of KNM-OG 45500 exhibits similarities with Early Pleistocene fossils from Eurasia and Africa that are assigned to H. erectus sensu lato (s.l.). Its size, on the other hand, is notably smaller than most other Homo erectus fossils and modern humans and similar to the specimens from Dmanisi (Georgia) and to Homo naledi. Taken together, our analyses of the frontal bone suggest a taxonomic attribution of KNM-OG 45500 to H. erectus s.l. and extend even further the range of size variability associated with this taxon around 900 Ka BP.