Neanderthals: fossil evidence and DNA

Neanderthals inhabited Western Eurasia from approximately 300 to 30 thousand years ago (ka). They are distinguished by a unique combination of anatomical traits, and are commonly associated with Middle Paleolithic lithic industries. Current consensus among paleoanthropologists is that they represented a separate Eurasian human lineage, which evolved in isolation from the rest of the Old World and which shared a common ancestor with modern humans in the Middle Pleistocene. It is thought that some aspects of the distinctive Neanderthal anatomy evolved in response to selection related to the extreme cold of the European glacial cycles. Nevertheless, genetic drift seems to be partially responsible for the evolution of these traits. The last appearance of Neanderthals in the fossil record ca. 30 ka BP dates a few millennia after the first appearance of modern humans in Europe. The retrieval of ancient mitochondrial and, more recently, nuclear DNA from Neanderthal fossil puts us in the unique position to combine fossil with genetic evidence to address questions about their evolution, paleobiology and eventual fate.     

Middle eastern origin model forHomo sapiens (Moderns & Neanderthals), language and modern behaviour

A new model may resolve the problem of when and where did appear anatomically modern humans. According to this model, Neanderthals were probably neither our ancestor nor different species.Homo sapiens appeared probably in the Middle East, approximately 150 ka ago and differentiated to anatomically modern humans and Neanderthals because of the genetic programme. The fossils older than 150 ka are probably not Neanderthal such as Zuttiyeh and Biache-Saint-Vaast specimens. Cultural capacities of Neanderthals were probably equivalent to Moderns. Most of pre-Homo sapiens populations may be extinct without replacement byHomo sapiens. Language and modern behaviour should have arisen with our own species.     

Using genetic evidence to evaluate four palaeoanthropological hypotheses for the timing of Neanderthal and modern human origins

A better understanding of the evolutionary relationship between modern humans and Neanderthals is essential for improving the resolution of hominin phylogenetic hypotheses. Currently, four distinct chronologies for the timing of population divergence are available, ranging from the late Middle Pleistocene to the late Early Pleistocene, each based on different interpretations of hominin taxonomy. Genetic data can present an independent estimate of the evolutionary timescale involved, making it possible to distinguish between these competing models of hominin evolution. We analysed five dated Neanderthal mitochondrial genomes, together with those of 54 modern humans, and inferred a genetic chronology using multiple age calibrations. Our mean date estimates are consistent with a process of genetic divergence within an ancestral population, commencing approximately 410-440 ka. These results suggest that a reappraisal of key elements in the Pleistocene hominin fossil record may now be required.     

The Vindija Neanderthal scapular glenoid fossa: comparative shape analysis suggests evo-devo changes among Neanderthals

Although the shape of the scapular glenoid fossa (SGF) may be influenced by epigenetic and developmental factors, there appears to be strong genetic control over its overall form, such that variation within and between hominin taxa in SGF shape may contain information about their evolutionary histories. Here we present the results of a geometric morphometric study of the SGF of the Neanderthal Vi-209 from Vindjia Cave (Croatia), relative to samples of Plio-Pleistocene, later Pleistocene, and recent hominins. Variation in overall SGF shape follows a chronological trend from the plesiomorphic condition seen in Australopithecus to modern humans, with pre-modern species of the genus Homo exhibiting intermediate morphologies. Change in body size across this temporal series is not linearly directional, which argues against static allometry as an explanation. However, life history and developmental rates change directionally across the series, suggesting an ontogenetic effect on the observed changes in shape (ontogenetic allometry). Within this framework, the morphospace occupied by the Neanderthals exhibits a discontinuous distribution. The Vindija SGF and those of the later Near Eastern Neanderthals (Kebara and Shanidar) approach the modern condition and are somewhat segregated from both northwestern European (Neandertal and La Ferrassie) and early Mediterranean Neanderthals (Krapina and Tabun). Although more than one scenario may account for the pattern seen in the Neanderthals, the data is consistent with palaeogenetic evidence suggesting low levels of gene flow between Neanderthals and modern humans in the Near East after ca. 120-100 ka (thousands of years ago) (with subsequent introgression of modern human alleles into eastern and central Europe). Thus, in keeping with previous analyses that document some modern human features in the Vindija Neanderthals, the Vindija G₃ sample should not be seen as representative of ‘classic’ - that is, unadmixed, pre-contact - Neanderthal morphology.     

Quantitative analysis of Neanderthal temporal bone morphology using three-dimensional geometric morphometrics

The temporal bone is the location of several traits thought to differentiate Neanderthals from modern humans, including some proposed Neanderthal-derived traits. Most of these, however, are difficult to measure and are usually described qualitatively. This study applied the techniques of geometric morphometrics to the complex morphology of the temporal bone, in order to quantify the differences observed between Neanderthal and modern human anatomy. Two hundred and seventy modern human crania were measured, representing 9 populations of 30 individuals each, and spanning the extremes of the modern human geographical range. Twelve Neanderthal specimens, as well as Reilingen, Kabwe, Skhul 5, Qafzeh 9, and 4 Late Paleolithic European specimens, were included in the fossil sample. The data were collected in the form of three-dimensional (3-D) landmark coordinates, and specimen configurations were superimposed using generalized Procrustes analysis. The fitted coordinates were then analyzed by an array of multivariate statistical methods, including principal components analysis, canonical variates analysis, and Mahalanobis D(2). The temporal bone landmark analysis was very successful in separating Neanderthals from modern humans. Neanderthals were separated from modern humans in both the principal components and canonical variates analyses. They were much further in Mahalanobis distances from all modern human populations than any two modern human groups were from each other. Most of the previously described temporal bone traits contributed to this separation.     

Evolution of middle-late Pleistocene human cranio-facial form: A 3-D approach

The classification and phylogenetic relationships of the middle Pleistocene human fossil record remains one of the most intractable problems in paleoanthropology. Several authors have noted broad resemblances between European and African fossils from this period, suggesting a single taxon ancestral to both modern humans and Neanderthals. Others point out ‘incipient’ Neanderthal features in the morphology of the European sample and have argued for their inclusion in the Neanderthal lineage exclusively, following a model of accretionary evolution of Neanderthals. We approach these questions using geometric morphometric methods which allow the intuitive visualization and quantification of features previously described qualitatively. We apply these techniques to evaluate proposed cranio-facial ‘incipient’ facial, vault, and basicranial traits in a middle-late Pleistocene European hominin sample when compared to a sample of the same time depth from Africa. Some of the features examined followed the predictions of the accretion model and relate the middle Pleistocene European material to the later Neanderthals. However, although our analysis showed a clear separation between Neanderthals and early/recent modern humans and morphological proximity between European specimens from OIS 7 to 3, it also shows that the European hominins from the first half of the middle Pleistocene still shared most of their cranio-facial architecture with their African contemporaries.     

The Neanderthal lower arm

Neanderthal forearms have been described as being very powerful. Different individual features in the lower arm bones have been described to distinguish Neanderthals from modern humans. In this study, the overall morphology of the radius and ulna is considered, and morphological differences among Neanderthals, Upper Paleolithic Homo sapiens and recent H. sapiens are described.Comparisons among populations were made using a combination of 3D geometric morphometrics and standard multivariate methods. Comparative material included all available complete radii and ulnae from Neanderthals, early H. sapiens and archaeological and recent human populations, representing a wide geographical and lifestyle range.There are few differences among the populations when features are considered individually. Neanderthals and early H. sapiens fell within the range of modern human variation. When the suite of measurements and shapes were analyzed, differences and similarities became apparent. The Neanderthal radius is more laterally curved, has a more medially placed radial tuberosity, a longer radial neck, a more antero-posteriorly ovoid head and a well-developed proximal interosseous crest. The Neanderthal ulna has a more anterior facing trochlear notch, a lower M. brachialis insertion, larger relative mid-shaft size and a more medio-lateral and antero-posterior sinusoidal shaft. The Neanderthal lower arm morphology reflects a strong cold-adapted short forearm. The forearms of H. sapiens are less powerful in pronation and supination. Many differences between Neanderthals and H. sapiens can be explained as a secondary consequence of the hyper-polar body proportions of the Neanderthals, but also as retentions of the primitive condition of other hominoids.     

The Neanderthal face is not cold adapted

Many morphological features of the Pleistocene fossil hominin Homo neanderthalensis, including the reputed large size of its paranasal sinuses, have been interpreted as adaptations to extreme cold, as some Neanderthals lived in Europe during glacial periods. This interpretation of sinus evolution rests on two assumptions: that increased craniofacial pneumatization is an adaptation to lower ambient temperatures, and that Neanderthals have relatively large sinuses. Analysis of humans, other primates, and rodents, however, suggests that the first assumption is suspect; at least the maxillary sinus undergoes a significant reduction in volume in extreme cold, in both wild and laboratory conditions. The second assumption, that Neanderthal sinuses are large, extensive, or even ‘hyperpneumatized,’ has held sway since the first specimen was described and has been interpreted as the causal explanation for some of the distinctive aspects of Neanderthal facial form, but has never been evaluated with respect to scaling. To test the latter assumption, previously published measurements from two-dimensional (2D) X-rays and new three-dimensional (3D) data from computed tomography (CT) of Neanderthals and temperate-climate European Homo sapiens are regressed against cranial size to determine the relative size of their sinuses. The 2D data reveal a degree of craniofacial pneumatization in Neanderthals that is both commensurate with the size of the cranium and comparable in scale with that seen in temperate climate H. sapiens. The 3D analysis of CT data from a smaller sample supports this conclusion. These results suggest that the distinctive Neanderthal face cannot be interpreted as a direct result of increased pneumatization, nor is it likely to be an adaptation to resist cold stress; an alternative explanation is thus required.     

The Neanderthal "chignon": variation, integration, and homology

The occipital bun ("chignon") is cited widely as a Neanderthal derived trait. It encompasses the posterior projection/convexity of the occipital squama and is associated with lambdoid flattening on the parietal. A 'hemibun' in some Upper Paleolithic Europeans is thought by some authors to indicate interbreeding between Neanderthals and early modern Europeans. However, 'bunning' is difficult to measure, and the term has been applied to a range of morphological patterns. Furthermore, its usefulness in phylogenetic reconstruction and its homologous status across modern and fossil humans have been disputed. We present a geometric morphometric study that quantitatively evaluates the chignon, assesses its usefulness in separating Neanderthals from modern humans, and its degree of similarity to Upper Paleolithic 'hemibuns.' We measured the three-dimensional coordinates of closely spaced points along the midsagittal plane from bregma to inion and of anatomical landmarks in a large series of recent human crania and several Middle and Late Pleistocene European and African fossils. These coordinate data were processed using the techniques of geometric morphometrics and analyzed with relative warps, canonical variates, and singular warps. Our results show no separation between Neanderthals and modern humans, including early modern Europeans, when the shape of the occipital plane midsagittal-profile is considered alone. On the other hand, Neanderthals are well separated from both recent and fossil modern humans when information about the occipital's relative position and relative size are also included. Furthermore, the occurrence of a highly convex and posteriorly projecting midline occipital profile (interpreted as the occipital bun) is highly correlated (>0.8) with a flat parietal midsagittal profile and with antero-superiorly positioned temporal bones across both our recent and our fossil human samples. We conclude that the shape of the occipital profile alone should not be considered an independent trait, as it is very tightly integrated with braincase shape. Our analysis does not support differences in integration of the posterior midsagittal profile and the cranial base in Pleistocene and recent humans.     

The Neanderthal taxonomic position: models of intra- and inter-specific craniofacial variation

The Neanderthal taxonomic position is a matter of wide disagreement among paleoanthropologists. Some workers consider this fossil human group to represent a different species, Homo neanderthalensis, while others see it as a subspecies of Homo sapiens. This study developed two models of morphological variation to be applied to a comparison between Neanderthals and modern humans: modern human populations provided a measure of intra-specific variation, while the species and subspecies of Pan provided measures of both intra- and inter-specific morphological differences. Although such an approach has been advocated strongly, it has not been systematically undertaken until recently. The techniques of geometric morphometrics were used to collect data in the form of three-dimensional coordinates of craniofacial landmarks. The data were processed using generalized procrustes analysis, and analyzed by an array of multivariate statistical methods, including principal components analysis, canonical variates analysis and Mahalanobis D(2). The morphological distances between Neanderthals and modern humans, and between Neanderthals and Late Paleolithic/early anatomically modern specimens, are consistently greater than the distances among recent human populations, and greater than the distances between the two chimpanzee species. Furthermore, no strong morphological similarities were found between Neanderthals and Late Paleolithic Europeans. This study does not find evidence for Neanderthal contribution to the evolution of modern Europeans. Results are consistent with the recognition of Neanderthals as a distinct species.     

Neanderthal skeleton from Tabun: U-series data by gamma-ray spectrometry

The Neanderthal hominid Tabun C1, found in Israel by Garrod & Bate, was attributed to either layer B or C of their stratigraphic sequence. We have used gamma-ray spectrometry to determine the²³⁰Th/²³⁴U and²³¹Pa/²³⁵U ratios of two bones from this skeleton, the mandible and a femur. The ages calculated from these ratios depend on the uranium uptake history of the bones. Assuming a model of early U (EU) uptake the age of the Tabun C1 mandible is 34±5 ka. The EU age of the femur is 19±2 ka. The femur may have experienced continuous (linear) U uptake which would give an age of 33±4 ka, in agreement with the mandible's EU age, but implies marked inhomogeneity in U uptake history at the site. These new age estimates for the skeleton suggest that it was younger than deposits of layer C. This apparent age is less than those of other Neanderthals found in Israel, and distinctly younger than the ages of the Skhul and Qafzeh burials. This suggests that Neanderthals did not necessarily coexist with the earliest modern humans in the region. All of the more complete Neanderthal fossils from Israel are now dated to the cool period of the last glacial cycle, suggesting that Neanderthals may have arrived in this region as a result of the southward expansion of their habitable range. The young age determined for the Tabun skeleton would suggest that Neanderthals survived as late in the Levant as they did in Europe.     

Comparison of dental measurement systems for taxonomic assignment of Neanderthal and modern human lower second deciduous molars

Traditional morphometric approaches for taxonomic assignment of Neanderthal and modern human dental remains are mainly characterized by caliper measurements of tooth crowns. Several studies have recently described differences in dental tissue proportions and enamel thickness between Neanderthal and modern human teeth. At least for the lower second deciduous molar (dm₂), a three-dimensional lateral relative enamel thickness index has been proposed for separating the two taxa. This index has the advantage over other measurements of being applicable to worn teeth because it ignores the occlusal aspect of the crown. Nevertheless, a comparative evaluation of traditional crown dimensions and lateral dental tissue proportion measurements for taxonomic assignment of Neanderthal and modern human dm₂s has not yet been performed.In this study, we compare various parameters gathered from the lateral aspects of the crown. These parameters include crown diameters, height of the lateral wall of the crown (lateral crown height = LCH), lateral enamel thickness, and dentine volume of the lateral wall, including the volume of the coronal pulp chamber (lateral dentine plus pulp volume = LDPV), in a 3D digital sample of Neanderthal and modern human dm₂s to evaluate their utility in separating the two taxa.The LDPV and the LCH allow us to discriminate between Neanderthals and modern humans with 88.5% and 92.3% accuracy, respectively. Though our results confirm that Neanderthal dm₂s have lower relative enamel thickness (RET) index compared with modern humans (p = 0.005), only 70% of the specimens were correctly classified on the basis of the RET index. We also emphasize that results of the lateral enamel thickness method depend on the magnitude of the interproximal wear. Accordingly, we suggest using the LCH or the LDPV to discriminate between Neanderthal and modern human dm₂s. These parameters are more independent of interproximal wear and loss of lateral enamel.     

The Mousterian child from Teshik‐Tash is a Neanderthal: A geometric morphometric study of the frontal bone

In the 1930s subadult hominin remains and Mousterian artifacts were discovered in the Teshik‐Tash cave in South Uzbekistan. Since then, the majority of the scientific community has interpreted Teshik‐Tash as a Neanderthal. However, some have considered aspects of the morphology of the Teshik‐Tash skull to be more similar to fossil modern humans such as those represented at Skhūl and Qafzeh, or to subadult Upper Paleolithic modern humans. Here we present a 3D geometric morphometric analysis of the Teshik‐Tash frontal bone in the context of developmental shape changes in recent modern humans, Neanderthals, and early modern humans. We assess the phenetic affinities of Teshik‐Tash to other subadult fossils, and use developmental simulations to predict possible adult shapes. We find that the morphology of the frontal bone places the Teshik‐Tash child close to other Neanderthal children and that the simulated adult shapes are closest to Neanderthal adults. Taken together with genetic data showing that Teshik‐Tash carried mtDNA of the Neanderthal type, as well as its occipital bun, and its shovel‐shaped upper incisors, these independent lines of evidence firmly place Teshik‐Tash among Neanderthals. Am J Phys Anthropol, 2012. © 2012 Wiley Periodicals, Inc.     

Femoral curvature in Neanderthals and modern humans: a 3D geometric morphometric analysis

Since their discovery, Neanderthals have been described as having a marked degree of anteroposterior curvature of the femoral shaft. Although initially believed to be pathological, subsequent discoveries of Neanderthal remains lead femoral curvature to be considered as a derived Neanderthal feature. A recent study on Neanderthals and middle and early Upper Palaeolithic modern humans found no differences in femoral curvature, but did not consider size-corrected curvature. Therefore, the objectives of this study were to use 3D morphometric landmark and semi-landmark analysis to quantify relative femoral curvature in Neanderthals, Upper Palaeolithic and recent modern humans, and to compare adult bone curvature as part of the overall femoral morphology among these populations.Comparisons among populations were made using geometric morphometrics (3D landmarks) and standard multivariate methods. Comparative material involved all available complete femora from Neanderthal and Upper Palaeolithic modern human, archaeological (Mesolithic, Neolithic, Medieval) and recent human populations representing a wide geographical and lifestyle range. There are significant differences in the anatomy of the femur between Neanderthals and modern humans. Neanderthals have more curved femora than modern humans. Early modern humans are most similar to recent modern humans in their anatomy. Femoral curvature is a good indicator of activity level and habitual loading of the lower limb, indicating higher activity levels in Neanderthals than modern humans. These differences contradict robusticity studies and the archaeological record, and would suggest that femoral morphology, and curvature in particular, in Neanderthals may not be explained by adult behavior alone and could be the result of genetic drift, natural selection or differences in behavior during ontogeny.     

Mandibular condyle traits in Neanderthals and other Homo: a comparative,correlative, and ontogenetic study

The relationship between the mandibular condyle and the crest of the mandibular notch (CMN) has historically entered into discussions of Neanderthal characteristics and was recently suggested to be autapomorphic in Neanderthals. The Neanderthal CMN has been described as intersecting the condyle in the middle, while the modern human CMN runs to the condyle's lateral end. A large lateral condylar tubercle (LCT) has also been observed in Neanderthals and thought to be related to medial (or less lateral) CMN position. In addition, the presence of a less lateral CMN early in ontogeny, as seen in the Amud 7 infant, has been argued to demonstrate great evolutionary divergence in Neanderthals. Using a scoring system for each trait, this study first examines the expression of CMN position and LCT size in 102 adult modern humans and in samples of Neanderthals and other fossil Homo. Then, CMN position is scored in 208 subadult modern humans to elucidate the ontogeny of this trait. Results show that CMN position is not autapomorphic in Neanderthals, but Neanderthals have significantly more CMNs in the least-lateral score category than does the modern human sample. Large LCTs are found to be strongly predictive of less lateral CMN position, although less lateral CMN position may exist in the absence of a large LCT. The complex ontogenetic pattern of CMN expression observed indicates that features of subadult and adult condylar morphology cannot be constructively compared without first considering subadult morphology on its own functional and developmental terms.     

Out of Africa and the evolution of human behavior

Twenty‐one years ago, a landmark exploration of mitochondrial DNA diversity popularized the idea of a recent African origin for all living humans. 1 The ancestral African population was estimated to have existed 200 ka (thousands of years ago) plus or minus a few tens of thousands of years. A corollary was that at some later date the fully modern African descendants of that population expanded to swamp or replace the Neanderthals and other nonmodern Eurasians. The basic concept soon became known as “Out of Africa,” after the Academy Award winning film (1985) that took its title, in turn, from Isak Dinesen's classic autobiography (1937). Many subsequent genetic analyses, including those of Ingman and coworkers 2 and Underhill and coworkers, 3 have reaffirmed the fundamental Out of Africa model. The fossil and archeological records also support it strongly. The fossil record implies that anatomically modern or near‐modern humans were present in Africa by 150 ka; the fossil and archeological records together indicate that modern Africans expanded to Eurasia beginning about 50 ka.     

ABO Genetic Variation in Neanderthals and Denisovans

Variation at the ABO locus was one of the earliest sources of data in the study of human population identity and history, and to this day remains widely genotyped due to its importance in blood and tissue transfusions. Here, we look at ABO blood type variants in our archaic relatives: Neanderthals and Denisovans. Our goal is to understand the genetic landscape of the ABO gene in archaic humans, and how it relates to modern human ABO variation. We found two Neanderthal variants of the O allele in the Siberian Neanderthals (O1 and O2), one of these variants is shared with an European Neanderthal, who is a heterozygote for this O1 variant and a rare cis-AB variant. The Denisovan individual is heterozygous for two variants of the O1 allele, functionally similar to variants found widely in modern humans. Perhaps more surprisingly, the O2 allele variant found in Siberian Neanderthals can be found at low frequencies in modern Europeans and Southeast Asians, and the O1 allele variant found in Siberian and European Neanderthal is also found at very low frequency in modern East Asians. Our genetic distance analyses suggest both alleles survive in modern humans due to inbreeding with Neanderthals. We find that the sequence backgrounds of the surviving Neanderthal-like O alleles in modern humans retain a higher sequence divergence than other surviving Neanderthal genome fragments, supporting a view of balancing selection operating in the Neanderthal ABO alleles by retaining highly diverse haplotypes compared with portions of the genome evolving neutrally.     

Modern humans did not admix with Neanderthals during their range expansion into Europe

The process by which the Neanderthals were replaced by modern humans between 42,000 and 30,000 before present is still intriguing. Although no Neanderthal mitochondrial DNA (mtDNA) lineage is found to date among several thousands of Europeans and in seven early modern Europeans, interbreeding rates as high as 25% could not be excluded between the two subspecies. In this study, we introduce a realistic model of the range expansion of early modern humans into Europe, and of their competition and potential admixture with local Neanderthals. Under this scenario, which explicitly models the dynamics of Neanderthals' replacement, we estimate that maximum interbreeding rates between the two populations should have been smaller than 0.1%. We indeed show that the absence of Neanderthal mtDNA sequences in Europe is compatible with at most 120 admixture events between the two populations despite a likely cohabitation time of more than 12,000 y. This extremely low number strongly suggests an almost complete sterility between Neanderthal females and modern human males, implying that the two populations were probably distinct biological species.