Increase on environmental seasonality through the European Early Pleistocene inferred from dental enamel hypoplasia.

An in-depth study of the Early Pleistocene European remains of Hippopotamus has allowed the first detailed description of the incidence and types of dental alterations related to palaeopathologies and potentially linked to climatic and environmental factors. The results of a long-term qualitative and quantitative assessment highlight the importance of nutrient deficiencies on the development of dental enamel hypoplasia in Hippopotamus. Glacial cyclicity and the resulting changes in humidity and plant community structure conditioned the local environments critical for the survival of this taxon. Two main intervals of putative constrained nutritionally restrictions were detected at ca. 1.8 Ma and ca. 0.86 Ma (i.e., MIS63 and MIS21, respectively). Statistical comparisons show an increase in the frequency of dental hypoplasia between these two chronological periods, thus reinforcing the idea of increased seasonality in the circum-Mediterranean environments during the Early Pleistocene.

The aorta in humans and African great apes, and cardiac output and metabolic levels in human evolution.

Humans have a larger energy budget than great apes, allowing the combination of the metabolically expensive traits that define our life history. This budget is ultimately related to the cardiac output, the product of the blood pumped from the ventricle and the number of heart beats per minute, a measure of the blood available for the whole organism physiological activity. To show the relationship between cardiac output and energy expenditure in hominid evolution, we study a surrogate measure of cardiac output, the aortic root diameter, in humans and great apes. When compared to gorillas and chimpanzees, humans present an increased body mass adjusted aortic root diameter. We also use data from the literature to show that over the human lifespan, cardiac output and total energy expenditure follow almost identical trajectories, with a marked increase during the period of brain growth, and a plateau during most of the adult life. The limited variation of adjusted cardiac output with sex, age and physical activity supports the compensation model of energy expenditure in humans. Finally, we present a first study of cardiac output in the skeleton through the study of the aortic impression in the vertebral bodies of the spine. It is absent in great apes, and present in humans and Neanderthals, large-brained hominins with an extended life cycle. An increased adjusted cardiac output, underlying higher total energy expenditure, would have been a key process in human evolution.

Three-Dimensional Comparative Study of Human Bipartite Scaphoids and the Os Centrale of the Wrist in Neandertals and Non-Human Anthropoid Primates.

In humans, bipartite scaphoid still does not differentiate clearly from traumatic non-union of the scaphoid. To aid diagnosis, we sought to analyze the main geometrical similarities among bipartite scaphoids from primate species with fused and unfused scaphoid centrales. Four human embryos, four cases of adult humans with bipartite scaphoid, twelve adult specimens of other extant anthropoid primates, and two Neandertal scaphoid specimens were included in this study. Three-dimensional polygon models of the scaphoid and os centrale were generated from CT scan, micro-CT scan, or histological sections. A 3D comparative study of the morphological and morphometrical parameters was performed using the MSC Patran software. The os centrale was smaller than the scaphoid in all specimens and its shape was elongated in the anteroposterior scaphoid direction. The position of the os centrale centroid compared to the scaphoid using direction vectors had a strong orientation along the proximodistal axis in all species. The main morphological feature of bipartite scaphoid was the continuity of the scaphoid from its proximal pole to its tubercule along the anteroposterior axis. In all specimens, if the os centrale was removed, the scaphoid still appeared normal and whole. The bipartite scaphoid in adult humans shares geometrical analogies with monkeys and orangutans, human embryos, and Neandertals. Morphological and morphometrical features identified in this study are useful to differentiate bipartite scaphoid from scaphoid pseudarthrosis. All other criteria suggested in the past lead to misdiagnosis.

Comparative anatomy and 3D geometric morphometrics of the El Sidrón atlases (C1).

The first cervical vertebra (atlas, C1) is an important element of the vertebral column because it connects the cranial base with the cervical column, thus helping to maintain head posture and contributing to neck mobility. However, few atlases are preserved in the fossil record because of the fragility of this vertebra. Consequently, only eight well-preserved atlases from adult Neandertals have been recovered and described. Here, we present nine new atlas remains from the El Sidrón Neandertal site (Asturias, Spain), two of which (SD-1643 and SD-1605/1595) are sufficiently well preserved to allow for a detailed comparative and three-dimensional geometric morphometric analysis. We compared standard linear measurements of SD-1643 and SD-1605/1595 with those of other Neandertal atlases and carried out three-dimensional geometric morphometric analyses to compare size and shape of SD-1643 and SD-1605/1595 with those of 28 Pan (Pan troglodytes and Pan paniscus), a broad comparative sample of 55 anatomically modern humans from African and European populations, and other fossil hominins (Neandertals, Homo antecessor, Paranthropus boisei). The El Sidrón atlas fossils show typical features of the Neandertal atlas morphology, such as caudal projection of the anterior tubercle, gracility of both the posterior tubercle and the tuberosity for the insertion of the transverse ligament, and an anteroposteriorly elongated neural canal. Furthermore, when compared with atlases from the other taxa, Neandertals exhibit species-specific features of atlas morphology including a relatively lower lateral mass height, relatively narrower transverse foramina, and flatter and more horizontally oriented articular facets. Some of these features fit with previous suggestions of shorter overall length of the cervical spine and potential differences in craniocervical posture and mobility. Our results may support a different spinopelvic alignment in this species, as the atlas morphology suggests reduced cervical lordosis.

The evolutionary history of Neanderthal and Denisovan Y chromosomes.

Ancient DNA has provided new insights into many aspects of human history. However, we lack comprehensive studies of the Y chromosomes of Denisovans and Neanderthals because the majority of specimens that have been sequenced to sufficient coverage are female. Sequencing Y chromosomes from two Denisovans and three Neanderthals shows that the Y chromosomes of Denisovans split around 700 thousand years ago from a lineage shared by Neanderthals and modern human Y chromosomes, which diverged from each other around 370 thousand years ago. The phylogenetic relationships of archaic and modern human Y chromosomes differ from the population relationships inferred from the autosomal genomes and mirror mitochondrial DNA phylogenies, indicating replacement of both the mitochondrial and Y chromosomal gene pools in late Neanderthals. This replacement is plausible if the low effective population size of Neanderthals resulted in an increased genetic load in Neanderthals relative to modern humans.

The position of Australopithecus sediba within fossil hominin hand use diversity.

The human lineage is marked by a transition in hand use, from locomotion towards increasingly dexterous manipulation, concomitant with bipedalism. The forceful precision grips used by modern humans probably evolved in the context of tool manufacture and use, but when and how many times hominin hands became principally manipulative remains unresolved. We analyse metacarpal trabecular and cortical bone, which provide insight into behaviour during an individual's life, to demonstrate previously unrecognized diversity in hominin hand use. The metacarpals of the palm in Australopithecus sediba have trabecular morphology most like orangutans and consistent with locomotor power-grasping with the fingers, while that of the thumb is consistent with human-like manipulation. This internal morphology is the first record of behaviour consistent with a hominin that used its hand for both arboreal locomotion and human-like manipulation. This hand use is distinct from other fossil hominins in this study, including A. afarensis and A. africanus.

Analyses of the neandertal patellae from El Sidrón (Asturias, Spain) with implications for the evolution of body form in Homo.

The evolution of the body form in Homo and its potential morphological connection to the arrangement of different skeletal systems is of major interest in human evolution. Patella morphology as part of the knee is potentially influenced by body form. Here, we describe for the first time the patellae remains recovered at El Sidrón Neandertal site and analyze them in a comparative evolutionary framework. We aim to clarify whether morphometric features frequently observed in Neandertal and modern human patellae are retained from a primitive anatomical arrangement or whether they represent derived features (apomorphies). For this purpose, we combine analyses of discrete features, classic anthropological measurements, and 3D geometric morphometrics based on generalized Procrustes analysis, mean size and shape comparisons, and principal components analysis. We found a size increment of the patella in hominin evolution, with large species showing a larger patella. Modern humans and Neandertals exhibit overall larger patellae, with maximum values observed in the latter, likely as a consequence of their broader body shape. Also, some Neandertals display a thicker patella, which has been linked to larger quadriceps muscles. However, Neandertals retain a primitive morphology in their patellar articular surfaces, with similar-sized lateral and medial articular facets, leading to a more symmetrical internal face. This feature is inherited from a primitive Homo ancestor and suggests a different configuration of the knee in Neandertals. Conversely, Homo sapiens exhibits an autoapomorphic patellar anatomy with expanded lateral articular facets. We propose that these distinct configurations of the patella within Homo may be a consequence of different body forms rather than specific functional adaptations of the knee. Thus, the slender body form of modern humans may entail a medial reorientation of the tibial tuberosity (patellar ligament), allowing lateral surface expansion. These anatomical evolutionary variations may involve subtle secondary differences in bipedalism within Homo.

The study of the lower limb entheses in the Neanderthal sample from El Sidrón (Asturias, Spain): How much musculoskeletal variability did Neanderthals accumulate?

Entheses have rarely been systematically studied in the field of human evolution. However, the investigation of their morphological variability (e.g., robusticity) could provide new insight into their evolutionary significance in the European Neanderthal populations. The aim of this work is to study the entheses and joint features of the lower limbs of El Sidrón Neanderthals (Spain; 49 ka), using standardized scoring methods developed on modern samples. Paleobiology, growth, and development of both juveniles and adults from El Sidrón are studied and compared with those of Krapina Neanderthals (Croatia, 130 ka) and extant humans. The morphological patterns of the gluteus maximus and vastus intermedius entheses in El Sidrón, Krapina, and modern humans differ from one another. Both Neanderthal groups show a definite enthesis design for the gluteus maximus, with little intrapopulation variability with respect to modern humans, who are characterized by a wider range of morphological variability. The gluteus maximus enthesis in the El Sidrón sample shows the osseous features of fibrous entheses, as in modern humans, whereas the Krapina sample shows the aspects of fibrocartilaginous ones. The morphology and anatomical pattern of this enthesis has already been established during growth in all three human groups. One of two and three of five adult femurs from El Sidrón and from Krapina, respectively, show the imprint of the vastus intermedius, which is absent among juveniles from those Neanderthal samples and in modern samples. The scant intrapopulation and the high interpopulation variability in the two Neanderthal samples is likely due to a long-term history of small, isolated populations with high levels of inbreeding, who also lived in different ecological conditions. The comparison of different anatomical entheseal patterns (fibrous vs. fibrocartilaginous) in the Neanderthals and modern humans provides additional elements in the discussion of their functional and genetic origin.

Relationship between vertical facial pattern and brain structure and shape.

OBJECTIVES: Dolichofacial (long-faced) and brachyfacial (short-faced) individuals show specific and well-differentiated craniofacial morphology. Here, we hypothesise that differences in the basicranial orientation and topology between dolicho- and brachyfacial subjects could be associated with differences in the supporting brain tissues. MATERIAL AND METHODS: Brain volumes (total intracranial, grey matter, and white matter volume), cortical thickness, and the volumes and shapes of fifteen subcortical nuclei were assessed on the basis of magnetic resonance imaging in 185 subjects. Global, voxel-wise and shape analyses, as well as multiple regression models, were generated to evaluate the association between vertical facial variations (dolicho- and brachyfacial spectrum) and brain morphology. RESULTS: Several differences in brain anatomy between dolicho- and brachyfacial subjects, along with relevant associations between vertical facial indices and brain structure and shape, were found. The most relevant finding of this study is related to the strong association of vertical facial indices with the volumes and shapes of subcortical nuclei, as the dolichofacial pattern increased, the bilateral hippocampus and brain stem expanded, while the left caudate, right pallidus, right amygdala, and right accumbens decreased in volume. CONCLUSIONS: Long- and short-faced human subjects present differences in brain structure and shape. CLINICAL SIGNIFICANT: The results of our study increase the clinician's knowledge about brain structure in dolicho- and brachyfacial patients. The findings could be of interest since the affected brain areas are involved in higher cognitive functions in humans, including language, memory, and attention.

First continuous pre-Jaramillo to Jaramillo terrestrial vertebrate succession from Europe.

In this paper, the early Pleistocene small vertebrate sequence of Quibas-Sima (Quibas karstic complex, Murcia, SE Spain) is presented. The available magnetostratigraphic information together with the small vertebrate association, allow to reliably constrain the age of the different units. The basal unit of the section has recorded a reversed polarity assigned to the pre-Jaramillo Matuyama (C1r.2r, i.e., between 1.2 and 1.07 Ma). The intermediate units have recorded a normal polarity correlated directly with the Jaramillo subchron (C1r.1n, between 1.07 and 0.99 Ma), while the upper units record the post-Jaramillo reverse polarity (C1r.1r, i.e., between 0.99 and 0.78). Jaramillo subchron is especially significant regarding the earliest hominin dispersal in Western Europe. However, vertebrate faunas unambiguously correlatable with Jaramillo subchron are extremely rare in Europe. Thereby, the study of the Quibas-Sima sequence allows to characterize the vertebrate association synchronous to this paleomagnetic episode in southern Iberian Peninsula, and contributes to increase knowledge of the biotic and climatic events that took place in southern Europe at the beginning of the Early-Middle Pleistocene transition, prior to the Matuyama-Brunhes boundary. A continuous small vertebrate succession has been reported, including representatives of the families Bufonidae, Pelodytidae, Testudinidae, Gekkonidae, Blanidae, Lacertidae, Colubridae, Viperidae, Soricidae, Erinaceidae, Rhinolophidae, Vespertilionidae, Muridae, Gliridae, Sciuridae, Leporidae and Ochotonidae The ecological affinities of the faunal association suggest a progressive reduction in forest cover in the onset of the Jaramillo subchron.

Ribcage measurements indicate greater lung capacity in Neanderthals and Lower Pleistocene hominins compared to modern humans.

Our most recent fossil relatives, the Neanderthals, had a large brain and a very heavy body compared to modern humans. This type of body requires high levels of energetic intake. While food (meat and fat consumption) is a source of energy, oxygen via respiration is also necessary for metabolism. We would therefore expect Neanderthals to have large respiratory capacities. Here we estimate the pulmonary capacities of Neanderthals, based on costal measurements and physiological data from a modern human comparative sample. The Kebara 2 male had a lung volume of about 9.04 l; Tabun C1, a female individual, a lung volume of 5.85 l; and a Neanderthal from the El Sidrón site, a lung volume of 9.03 l. These volumes are approximately 20% greater than the corresponding volumes of modern humans of the same body size and sex. These results show that the Neanderthal body was highly sensitive to energy supply.

Over 100 years of Krapina: New insights into the Neanderthal thorax from the study of rib cross-sectional morphology.

The Krapina costal sample was studied by Gorjanovic-Kramberger in the early twentieth century. He pointed out unique features in the sample such as the rounder rib cross-section, which was recently confirmed in other Neanderthal specimens. Round rib cross-sections are characteristic of Homo ergaster, suggesting this may be plesiomorphic for Pleistocene Homo, but it is unknown whether Homo antecessor also had this rib shape. Furthermore, the influence of allometry on the cross-sectional shape of ribs is still unknown. The large costal sample from Krapina allows us to address these issues. We quantified cross-section morphology at the midshaft throughout a closed curve of one landmark and nine sliding semilandmarks in the Krapina costal remains (n = 7), as well as in other Neanderthals (n = 50), H. antecessor (n = 3) and modern humans, both fossil (n = 12) and recent (n = 160). We used principal components analysis and mean comparisons to explore interspecific differences, regression analysis to investigate allometry, and partial least squares analysis to examine covariation of cross-section shape and overall rib morphology. Neanderthal cross-sections tended to be larger than those of recent humans except for the Krapina and Tabun remains. Regarding shape, inter-group differences were found only in the diaphragmatic thorax, where Neanderthal and H. antecessor ribs were statistically significantly rounder than those of modern humans. Allometry accounted for covariation of size on shape, but the Neandertal and modern human trajectories had different slopes. While our results based on the Krapina costal sample are similar to previous findings, we also make several new insights: 1) the cross-section morphology observed in Neanderthals was probably present in H. antecessor, albeit less marked; 2) the distinct roundness of Neanderthal cross-sections is not related to size; 3) rounder cross-sections are correlated with ribs presenting less curvature in cranial view and a low degree of torsion in recent humans. These results are important for the interpretation of fragmentary Neanderthal costal remains, and the fact that the differences are marked only in the diaphragmatic thorax could have implications for breathing kinematics.

Primary visual cortex in neandertals as revealed from the occipital remains from the El Sidrón site, with emphasis on the new SD-2300 specimen.

The comparative analysis of the endocranial surface of the El Sidrón new occipital fragment SD-2300 shows meaningful differences in the configuration of the occipital pole region between neandertals and anatomically modern humans (AMH). The particular asymmetries found in neandertals in the venous sinus drainage and the petalial patterns are recognizable in this new specimen as well. In addition, the supra- and infracalcarine fossae of the occipital pole region appear to deviate obliquely from the mid-line when compared with sapiens. Due to the excellent preservation conditions of SD-2300, the main sulci and gyri of the occipital pole area have been identified, this degree of detail being uncommon in a fossil specimen; in general, the gyrification pattern is similar to AMH, but with some notable differences. Particularly interesting is the description of the lunate and the calcarine sulci. The lunate sulcus is located close to the occipital pole, in a similar posterior position to in other Homo species. Regarding the calcarine sulcus, there are significant differences in the primary visual cortex, with the V1 area, or Brodmann area 17, being larger in Homo neanderthalensis than in Homo sapiens. This may lead to greater visual acuity in neandertals than in sapiens.

Response to Comment on "The growth pattern of Neandertals, reconstructed from a juvenile skeleton from El Sidrón (Spain)".

The comment by DeSilva challenges our suggestion that brain growth of the El Sidrón J1 Neandertal was still incomplete at 7.7 years of age. Evidence suggests that endocranial volume is likely to represent less than 90% adult size at El Sidrón as well as Neandertal male plus Krapina samples, in line with further evidence from endocranial surface histology and dural sinus groove size.

New Neandertal wrist bones from El Sidrón, Spain (1994-2009).

Twenty-nine carpal bones of Homo neanderthalensis have been recovered from the site of El Sidrón (Asturias, Spain) during excavations between 1994 and 2009, alongside ∼2500 other Neandertal skeletal elements dated to ∼49,000 years ago. All bones of the wrist are represented, including adult scaphoids (n = 6), lunates (n = 2), triquetra (n = 4), pisiforms (n = 2), trapezia (n = 2), trapezoids (n = 5), capitates (n = 5), and hamates (n = 2), as well as one fragmentary and possibly juvenile scaphoid. Several of these carpals appear to belong to the complete right wrist of a single individual. Here we provide qualitative and quantitative morphological descriptions of these carpals, within a comparative context of other European and Near Eastern Neandertals, early and recent Homo sapiens, and other fossil hominins, including Homo antecessor, Homo naledi, and australopiths. Overall, the El Sidrón carpals show characteristics that typically distinguish Neandertals from H. sapiens, such as a relatively flat first metacarpal facet on the trapezium and a more laterally oriented second metacarpal facet on the capitate. However, there are some distinctive features of the El Sidrón carpals compared with most other Neandertals. For example, the tubercle of the trapezium is small with limited projection, while the scaphoid tubercle and hamate hamulus are among the largest seen in other Neandertals. Furthermore, three of the six adult scaphoids show a distinctive os-centrale portion, while another is a bipartite scaphoid with a truncated tubercle. The high frequency of rare carpal morphologies supports other evidence of a close genetic relationship among the Neandertals found at El Sidrón.

Right-handed fossil humans.

Fossil hominids often processed material held between their upper and lower teeth. Pulling with one hand and cutting with the other, they occasionally left impact cut marks on the lip (labial) surface of their incisors and canines. From these actions, it possible to determine the dominant hand used. The frequency of these oblique striations in an array of fossil hominins documents the typically modern pattern of 9 right- to 1 left-hander. This ratio among living Homo sapiens differs from that among chimpanzees and bonobos and more distant primate relatives. Together, all studies of living people affirm that dominant right-handedness is a uniquely modern human trait. The same pattern extends deep into our past. Thus far, the majority of inferred right-handed fossils come from Europe, but a single maxilla from a Homo habilis, OH-65, shows a predominance of right oblique scratches, thus extending right-handedness into the early Pleistocene of Africa. Other studies show right-handedness in more recent African, Chinese, and Levantine fossils, but the sample compiled for non-European fossil specimens remains small. Fossil specimens from Sima del los Huesos and a variety of European Neandertal sites are predominately right-handed. We argue the 9:1 handedness ratio in Neandertals and the earlier inhabitants of Europe constitutes evidence for a modern pattern of handedness well before the appearance of modern Homo sapiens.

The costal remains of the El Sidrón Neanderthal site (Asturias, northern Spain) and their importance for understanding Neanderthal thorax morphology.

The study of the Neanderthal thorax has attracted the attention of the scientific community for more than a century. It is agreed that Neanderthals have a more capacious thorax than modern humans, but whether this was caused by a medio-lateral or an antero-posterior expansion of the thorax is still debated, and is key to understanding breathing biomechanics and body shape in Neanderthals. The fragile nature of ribs, the metameric structure of the thorax and difficulties in quantifying thorax morphology all contribute to uncertainty regarding precise aspects of Neanderthal thoracic shape. The El Sidrón site has yielded costal remains from the upper to the lower thorax, as well as several proximal rib ends (frequently missing in the Neanderthal record), which help to shed light on Neanderthal thorax shape. We compared the El Sidrón costal elements with ribs from recent modern humans as well as with fossil modern humans and other Neanderthals through traditional morphometric methods and 3D geometric morphometrics, combined with missing data estimation and virtual reconstruction (at the 1st, 5th and 11th costal levels). Our results show that Neanderthals have larger rib heads and articular tubercles than their modern human counterparts. Neanderthal 1st ribs are smaller than in modern humans, whereas 5th and 11th ribs are considerably larger. When we articulated mean ribs (size and shape) with their corresponding vertebral elements, we observed that compared to modern humans the Neanderthal thorax is medio-laterally expanded at every level, especially at T5 and T11. Therefore, in the light of evidence from the El Sidrón costal remains, we hypothesize that the volumetric expansion of the Neanderthal thorax proposed by previous authors would mainly be produced by a medio-lateral expansion of the thorax.