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.     

Neanderthal infant and adult infracranial remains from Marillac (Charente,France)

At the site of Marillac, near the Ligonne River in Marillac‐le‐Franc (Charente, France), a remarkable stratigraphic sequence has yielded a wealth of archaeological information, palaeoenvironmental data, as well as faunal and human remains. Marillac must have been a sinkhole used by Neanderthal groups as a hunting camp during MIS 4 (TL date 57,600 ± 4,600BP), where Quina Mousterian lithics and fragmented bones of reindeer predominate. This article describes three infracranial skeleton fragments. Two of them are from adults and consist of the incomplete shafts of a right radius (Marillac 24) and a left fibula (Marillac 26). The third fragment is the diaphysis of the right femur of an immature individual (Marillac 25), the size and shape of which resembles those from Teshik‐Tash and could be assigned to a child of a similar age. The three fossils have been compared with the remains of other Neanderthals or anatomically Modern Humans (AMH). Furthermore, the comparison of the infantile femora, Marillac 25 and Teshik‐Tash, with the remains of several European children from the early Middle Ages clearly demonstrates the robustness and rounded shape of both Neanderthal diaphyses. Evidence of peri‐mortem manipulations have been identified on all three bones, with spiral fractures, percussion pits and, in the case of the radius and femur, unquestionable cutmarks made with flint implements, probably during defleshing. Traces of periostosis appear on the fibula fragment and on the immature femoral diaphysis, although their aetiology remains unknown. Am J Phys Anthropol 155:99–113, 2014. © 2014 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.     

Evaluating developmental shape changes in Homo antecessor subadult facial morphology

The fossil ATD6-69 from Atapuerca, Spain, dated to ca. 900 ka (thousands of years ago) has been suggested to mark the earliest appearance of modern human facial features. However, this specimen is a subadult and the interpretation of its morphology remains controversial, because it is unclear how developmental shape changes would affect the features that link ATD6-69 to modern humans. Here we analyze ATD6-69 in an evolutionary and developmental context. Our modern human sample comprises cross-sectional growth series from four populations. The fossil sample covers human specimens from the Pleistocene to the Upper Paleolithic, and includes several subadult Early Pleistocene humans and Neanderthals. We digitized landmarks and semilandmarks on surface and CT scans and analyzed the Procrustes shape coordinates using multivariate statistics. Ontogenetic allometric trajectories and developmental simulations were employed in order to identify growth patterns and to visualize potential adult shapes of ATD6-69. We show that facial differences between modern and archaic humans are not exclusively allometric. We find that while postnatal growth further accentuates the differences in facial features between Neanderthals and modern humans, those features that have been suggested to link ATD6-69's morphology to modern humans would not have been significantly altered in the course of subsequent development. In particular, the infraorbital depression on this specimen would have persisted into adulthood. However, many of the facial features that ATD6-69 shares with modern humans can be considered to be part of a generalized pattern of facial architecture. Our results present a complex picture regarding the polarity of facial features and demonstrate that some modern human-like facial morphology is intermittently present in Middle Pleistocene humans. We suggest that some of the facial features that characterize recent modern humans may have developed multiple times in human evolution.     

The bony labyrinth of Neanderthals

This paper presents a comprehensive comparative analysis of the Neanderthal bony labyrinth, a structure located inside the petrous temporal bone. Fifteen Neanderthal specimens are compared with a Holocene human sample, as well as with a small number of European Middle Pleistocene hominins, and early anatomically modern and European Upper Palaeolithic humans. Compared with Holocene humans the bony labyrinth of Neanderthals can be characterized by an anterior semicircular canal arc which is smaller in absolute and relative size, is relatively narrow, and shows more torsion. The posterior semicircular canal arc is smaller in absolute and relative size as well, it is more circular in shape, and is positioned more inferiorly relative to the lateral canal plane. The lateral semicircular canal arc is absolutely and relatively larger. Finally, the Neanderthal ampullar line is more vertically inclined relative to the planar orientation of the lateral canal. The European Upper Palaeolithic and early modern humans are most similar, although not fully identical to Holocene humans in labyrinthine morphology. The European Middle Pleistocene hominins show the typical semicircular canal morphology of Neanderthals, with the exception of the arc shape and inferiorly position of the posterior canal and the strongly inclined ampullar line. The marked difference between the labyrinths of Neanderthals and modern humans can be used to assess the phylogenetic affinities of fragmentary temporal bone fossils. However, this application is limited by a degree of overlap between the morphologies. The typical shape of the Neanderthal labyrinth appears to mirror aspects of the surrounding petrous pyramid, and both may follow from the phylogenetic impact of Neanderthal brain morphology moulding the shape of the posterior cranial fossa. The functionally important arc sizes of the Neanderthal semicircular canals may reflect a pattern of head movements different from that of modern humans, possibly related to aspects of locomotor behaviour and the kinematic properties of their head and neck.     

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.     

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.     

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.     

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.     

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.     

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.     

Mugharet el'Aliya: Affinities of an enigmatic north African Aterian maxillary fragment

Objectives

This study uses a virtual framework to examine the left maxillary fragment of the juvenile fossil from Mugharet el'Aliya, Morocco, found in association with an Aterian lithic industry. Previously, this fossil had been ascribed to modern humans or the Neanderthal lineage based on its “archaic”/“Neanderthal-like” features and apparent large size. Here, we conducted a novel 3D shape comparative analysis of the maxillary fragment to clarify its taxonomic affinities with regard to its size and ontogeny.

Materials and Methods

Eighty Computed Tomography and surface scans representing ontogenetic samples of Homo sapiens and Homo neanderthalensis were used to capture species-specific differences. The toolkit of geometric morphometrics in combination with surface registration and an elastic iterative closest point algorithm were used to create a dataset of meshes with an identical number of corresponding vertices for the maxillae. Multivariate statistics were applied to Procrustes superimposed coordinates derived from the vertices of this dataset.

Results

Our analysis showed affinities of the Mugharet el'Aliya individual with our H. sapiens sample, especially with a subadult individual from Qafzeh. No size-independent affinities with Neanderthals of comparable dental age could be identified.

Discussion

Our results add to the evidence connecting fossils from western Asia, especially Qafzeh and Skhul, and the North African Aterian. Furthermore, Mugharet el'Aliya adds to our knowledge of the ontogenetic development of adult morphology that is frequently used to characterize hominin groups, for example, Neanderthals and modern humans.     

Obstetric implications of neanderthal robusticity and bone density

Neanderthal pelvic morphology is not well understood, despite the recent find and analysis of the Kebara 2 pelvis. Many of the proposed hypotheses focus on the possible need for a larger birth canal. A previously unexplored aspect involves possible direct obstetric implications of bone robusticity and density. These characteristics ocan affect obstetrics in modern humans, especially the molding of the neonate's head during parturition: engineering studies have shown that denser neonate cranial bones undergo less deformation, and thicker (more robust) cranial bones would also be expected to deform less during the birth process. These bone characteristics may also result in a less flexible birth canal. Thus, more robust or denser bones could result in the need for a larger birth canal or a smaller neonate head, due to decreased flexibility. Examples from modern populations are discussed and the conclusions applied to Neanderthals, who are known to have had high bone robusticity and may have had high bone density, given their heavy musculature. (A positive association between muscle mass and bone density has been observed repeatedly in modern humans.) We conclude that bone robusticity and density may have obstetrical implications for Neanderthals, with particular importance for neonate head molding during birth.     

Genome digging: insight into the mitochondrial genome of Homo

Background

A fraction of the Neanderthal mitochondrial genome sequence has a similarity with a 5,839-bp nuclear DNA sequence of mitochondrial origin (numt) on the human chromosome 1. This fact has never been interpreted. Although this phenomenon may be attributed to contamination and mosaic assembly of Neanderthal mtDNA from short sequencing reads, we explain the mysterious similarity by integration of this numt (mtAncestor-1) into the nuclear genome of the common ancestor of Neanderthals and modern humans not long before their reproductive split.

Principal Findings

Exploiting bioinformatics, we uncovered an additional numt (mtAncestor-2) with a high similarity to the Neanderthal mtDNA and indicated that both numts represent almost identical replicas of the mtDNA sequences ancestral to the mitochondrial genomes of Neanderthals and modern humans. In the proteins, encoded by mtDNA, the majority of amino acids distinguishing chimpanzees from humans and Neanderthals were acquired by the ancestral hominins. The overall rate of nonsynonymous evolution in Neanderthal mitochondrial protein-coding genes is not higher than in other lineages. The model incorporating the ancestral hominin mtDNA sequences estimates the average divergence age of the mtDNAs of Neanderthals and modern humans to be 450,000–485,000 years. The mtAncestor-1 and mtAncestor-2 sequences were incorporated into the nuclear genome approximately 620,000 years and 2,885,000 years ago, respectively.

Conclusions

This study provides the first insight into the evolution of the mitochondrial DNA in hominins ancestral to Neanderthals and humans. We hypothesize that mtAncestor-1 and mtAncestor-2 are likely to be molecular fossils of the mtDNAs of Homo heidelbergensis and a stem Homo lineage. The d_N/d_S dynamics suggests that the effective population size of extinct hominins was low. However, the hominin lineage ancestral to humans, Neanderthals and H. heidelbergensis, had a larger effective population size and possessed genetic diversity comparable with those of chimpanzee and gorilla.     

Neanderthals

Neanderthals are a group of fossil humans that inhabited Western Eurasia from approximately 300 to 30,000 years ago (ka). They vanished from the fossil record a few millennia after the first modern humans appeared in Europe (ca. 40 ka BP). They are characterized by a unique combination of distinctive anatomical features, and are found with stone tools of the Mousterian stone tool industry. Current consensus views them as a distinct Eurasian human lineage isolated from the rest of the Old World and sharing a common ancestor with modern humans sometime in the early Middle Pleistocene. The extreme cold of the European Ice Ages is considered at least partly responsible for the evolution of some of the distinctive Neanderthal anatomy, although other factors (functional demands, effects of chance in small populations) were probably also important. The causes for the Neanderthal extinction are not well understood. Worsening climate and competition with modern humans are implicated. Neanderthals were our sister species, much more closely related to us than the chimpanzees, our closest living relatives are today.     

Brief communication: dental development and enamel thickness in the Lakonis Neanderthal molar

Developmental and structural affinities between modern human and Neanderthal dental remains continue to be a subject of debate as well as their utility for informing assessments of life history and taxonomy. Excavation of the Middle Paleolithic cave site Lakonis in southern Greece has yielded a lower third molar (LKH 1). Here, we detail the crown development and enamel thickness of the distal cusps of the LKH 1 specimen, which has been classified as a Neanderthal based on the presence of an anterior fovea and mid-trigonid crest. Crown formation was determined using standard histological techniques, and enamel thickness was measured from a virtual plane of section. Developmental differences include thinner cuspal enamel and a lower periodicity than modern humans. Crown formation in the LKH 1 hypoconid is estimated to be 2.6-2.7 years, which is shorter than modern human times. The LKH 1 hypoconid also shows a more rapid overall crown extension rate than modern humans. Relative enamel thickness was approximately half that of a modern human sample mean; enamel on the distal cusps of modern human third molars is extremely thick in absolute and relative terms. These findings are consistent with recent studies that demonstrate differences in crown development, tissue proportions, and enamel thickness between Neanderthals and modern humans. Although overlap in some developmental variables may be found, the results of this and other studies suggest that Neanderthal molars formed in shorter periods of time than modern humans, due in part to thinner enamel and faster crown extension rates.