Publications by authors named "Marco de la Rasilla"

44 Publications

The evolutionary history of Neanderthal and Denisovan Y chromosomes.

Science 2020 09;369(6511):1653-1656

Department of Evolutionary Genetics, Max Planck Institute for Evolutionary Anthropology, D-04103 Leipzig, Germany.

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.
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http://dx.doi.org/10.1126/science.abb6460DOI Listing
September 2020

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

J Hum Evol 2020 04 5;141:102738. Epub 2020 Mar 5.

Group of Paleoanthropology MNCN-CSIC, Department of Paleobiology, Museo Nacional de Ciencias Naturales (CSIC), José Gutiérrez Abascal 2, Madrid, Spain.

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.
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http://dx.doi.org/10.1016/j.jhevol.2019.102738DOI Listing
April 2020

Chronological reassessment of the Middle to Upper Paleolithic transition and Early Upper Paleolithic cultures in Cantabrian Spain.

PLoS One 2018 18;13(4):e0194708. Epub 2018 Apr 18.

Department of Civil and Environmental Engineering, Imperial College London, London, United Kingdom.

Methodological advances in dating the Middle to Upper Paleolithic transition provide a better understanding of the replacement of local Neanderthal populations by Anatomically Modern Humans. Today we know that this replacement was not a single, pan-European event, but rather it took place at different times in different regions. Thus, local conditions could have played a role. Iberia represents a significant macro-region to study this process. Northern Atlantic Spain contains evidence of both Mousterian and Early Upper Paleolithic occupations, although most of them are not properly dated, thus hindering the chances of an adequate interpretation. Here we present 46 new radiocarbon dates conducted using ultrafiltration pre-treatment method of anthropogenically manipulated bones from 13 sites in the Cantabrian region containing Mousterian, Aurignacian and Gravettian levels, of which 30 are considered relevant. These dates, alongside previously reported ones, were integrated into a Bayesian age model to reconstruct an absolute timescale for the transitional period. According to it, the Mousterian disappeared in the region by 47.9-45.1ka cal BP, while the Châtelperronian lasted between 42.6k and 41.5ka cal BP. The Mousterian and Châtelperronian did not overlap, indicating that the latter might be either intrusive or an offshoot of the Mousterian. The new chronology also suggests that the Aurignacian appears between 43.3-40.5ka cal BP overlapping with the Châtelperronian, and ended around 34.6-33.1ka cal BP, after the Gravettian had already been established in the region. This evidence indicates that Neanderthals and AMH co-existed <1,000 years, with the caveat that no diagnostic human remains have been found with the latest Mousterian, Châtelperronian or earliest Aurignacian in Cantabrian Spain.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0194708PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5905894PMC
July 2018

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

Science 2018 03;359(6380)

Department of Cell and Developmental Biology, University College London, London WC1E 6BT, UK.

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.
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http://dx.doi.org/10.1126/science.aar3820DOI Listing
March 2018

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

J Hum Evol 2018 01 31;114:45-75. Epub 2017 Oct 31.

Área de Prehistoria Departamento de Historia, Universidad de Oviedo, Oviedo, Spain.

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.
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http://dx.doi.org/10.1016/j.jhevol.2017.09.007DOI Listing
January 2018

The growth pattern of Neandertals, reconstructed from a juvenile skeleton from El Sidrón (Spain).

Science 2017 09;357(6357):1282-1287

Department of Cell and Developmental Biology, University College London, Gower Street, London WC1E 6BT, UK.

Ontogenetic studies help us understand the processes of evolutionary change. Previous studies on Neandertals have focused mainly on dental development and inferred an accelerated pace of general growth. We report on a juvenile partial skeleton (El Sidrón J1) preserving cranio-dental and postcranial remains. We used dental histology to estimate the age at death to be 7.7 years. Maturation of most elements fell within the expected range of modern humans at this age. The exceptions were the atlas and mid-thoracic vertebrae, which remained at the 5- to 6-year stage of development. Furthermore, endocranial features suggest that brain growth was not yet completed. The vertebral maturation pattern and extended brain growth most likely reflect Neandertal physiology and ontogenetic energy constraints rather than any fundamental difference in the overall pace of growth in this extinct human.
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http://dx.doi.org/10.1126/science.aan6463DOI Listing
September 2017

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

J Hum Evol 2017 10 3;111:85-101. Epub 2017 Aug 3.

Paleoanthropology Group, Museo Nacional de Ciencias Naturales (CSIC), J. G. Abascal 2, 28006, Madrid, Spain.

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.
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http://dx.doi.org/10.1016/j.jhevol.2017.06.003DOI Listing
October 2017

Neandertal talus bones from El Sidrón site (Asturias, Spain): A 3D geometric morphometrics analysis.

Am J Phys Anthropol 2017 10 17;164(2):394-415. Epub 2017 Jul 17.

Área de Prehistoria, Department of History, Universidad de Oviedo. Calle Teniente Alfonso Martínez s/n, Oviedo, 33011, Spain.

Objectives: The El Sidrón tali sample is assessed in an evolutionary framework. We aim to explore the relationship between Neandertal talus morphology and body size/shape. We test the hypothesis 1: talar Neandertal traits are influenced by body size, and the hypothesis 2: shape variables independent of body size correspond to inherited primitive features.

Materials And Methods: We quantify 35 landmarks through 3D geometric morphometrics techniques to describe H. neanderthalensis-H. sapiens shape variation, by Mean Shape Comparisons, Principal Component, Phenetic Clusters, Minimum spanning tree analyses and partial least square and regression of talus shape on body variables. Shape variation correlated to body size is compared to Neandertals-Modern Humans (MH) evolutionary shape variation. The Neandertal sample is compared to early hominins.

Results: Neandertal talus presents trochlear hypertrophy, a larger equality of trochlear rims, a shorter neck, a more expanded head, curvature and an anterior location of the medial malleolar facet, an expanded and projected lateral malleolar facet and laterally expanded posterior calcaneal facet compared to MH.

Discussion: The Neandertal talocrural joint morphology is influenced by body size. The other Neandertal talus traits do not co-vary with it or not follow the same co-variation pattern as MH. Besides, the trochlear hypertrophy, the trochlear rims equality and the short neck could be inherited primitive features; the medial malleolar facet morphology could be an inherited primitive feature or a secondarily primitive trait; and the calcaneal posterior facet would be an autapomorphic feature of the Neandertal lineage.
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http://dx.doi.org/10.1002/ajpa.23280DOI Listing
October 2017

Three-dimensional morphometrics of thoracic vertebrae in Neandertals and the fossil evidence from El Sidrón (Asturias, Northern Spain).

J Hum Evol 2017 07 5;108:47-61. Epub 2017 May 5.

Paleoanthropology Group, Museo Nacional de Ciencias Naturales (CSIC), J. G. Abascal 2, 28006, Madrid, Spain.

Well preserved thoracic vertebrae of Neandertals are rare. However, such fossils are important as their three-dimensional (3D) spatial configuration can contribute to the understanding of the size and shape of the thoracic spine and the entire thorax. This is because the vertebral body and transverse processes provide the articulation and attachment sites for the ribs. Dorsal orientation of the transverse processes relative to the vertebral body also rotates the attached ribs in a way that could affect thorax width. Previous research indicates possible evidence for greater dorsal orientation of the transverse processes and small vertebral body heights in Neandertals, but their 3D vertebral structure has not yet been addressed. Here we present 15 new vertebral remains from the El Sidrón Neandertals (Asturias, Northern Spain) and used 3D geometric morphometrics to address the above issues by comparing two particularly well preserved El Sidrón remains (SD-1619, SD-1641) with thoracic vertebrae from other Neandertals and a sample of anatomically modern humans. Centroid sizes of El Sidrón vertebrae are within the human range. Neandertals have larger T1 and probably also T2. The El Sidrón vertebrae are similar in 3D shape to those of other Neandertals, which differ from Homo sapiens particularly in central-lower regions (T6-T10) of the thoracic spine. Differences include more dorsally and cranially oriented transverse processes, less caudally oriented spinous processes, and vertebral bodies that are anteroposteriorly and craniocaudally short. The results fit with current reconstructions of Neandertal thorax morphology.
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http://dx.doi.org/10.1016/j.jhevol.2017.03.008DOI Listing
July 2017

Neandertal and Denisovan DNA from Pleistocene sediments.

Science 2017 May 27;356(6338):605-608. Epub 2017 Apr 27.

Department of Evolutionary Genetics, Max Planck Institute for Evolutionary Anthropology, Deutscher Platz 6, 04103 Leipzig, Germany.

Although a rich record of Pleistocene human-associated archaeological assemblages exists, the scarcity of hominin fossils often impedes the understanding of which hominins occupied a site. Using targeted enrichment of mitochondrial DNA, we show that cave sediments represent a rich source of ancient mammalian DNA that often includes traces of hominin DNA, even at sites and in layers where no hominin remains have been discovered. By automation-assisted screening of numerous sediment samples, we detected Neandertal DNA in eight archaeological layers from four caves in Eurasia. In Denisova Cave, we retrieved Denisovan DNA in a Middle Pleistocene layer near the bottom of the stratigraphy. Our work opens the possibility of detecting the presence of hominin groups at sites and in areas where no skeletal remains are found.
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http://dx.doi.org/10.1126/science.aam9695DOI Listing
May 2017

Neanderthal behaviour, diet, and disease inferred from ancient DNA in dental calculus.

Nature 2017 04 8;544(7650):357-361. Epub 2017 Mar 8.

Australian Centre for Ancient DNA, School of Biological Sciences and The Environment Institute, University of Adelaide, Adelaide, South Australia, Australia.

Recent genomic data have revealed multiple interactions between Neanderthals and modern humans, but there is currently little genetic evidence regarding Neanderthal behaviour, diet, or disease. Here we describe the shotgun-sequencing of ancient DNA from five specimens of Neanderthal calcified dental plaque (calculus) and the characterization of regional differences in Neanderthal ecology. At Spy cave, Belgium, Neanderthal diet was heavily meat based and included woolly rhinoceros and wild sheep (mouflon), characteristic of a steppe environment. In contrast, no meat was detected in the diet of Neanderthals from El Sidrón cave, Spain, and dietary components of mushrooms, pine nuts, and moss reflected forest gathering. Differences in diet were also linked to an overall shift in the oral bacterial community (microbiota) and suggested that meat consumption contributed to substantial variation within Neanderthal microbiota. Evidence for self-medication was detected in an El Sidrón Neanderthal with a dental abscess and a chronic gastrointestinal pathogen (Enterocytozoon bieneusi). Metagenomic data from this individual also contained a nearly complete genome of the archaeal commensal Methanobrevibacter oralis (10.2× depth of coverage)-the oldest draft microbial genome generated to date, at around 48,000 years old. DNA preserved within dental calculus represents a notable source of information about the behaviour and health of ancient hominin specimens, as well as a unique system that is useful for the study of long-term microbial evolution.
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http://dx.doi.org/10.1038/nature21674DOI Listing
April 2017

Adult Neandertal clavicles from the El Sidrón site (Asturias, Spain) in the context of Homo pectoral girdle evolution.

J Hum Evol 2016 06 3;95:55-67. Epub 2016 May 3.

Área de Prehistoria, Department of History, Universidad de Oviedo, Calle Teniente Alfonso Martínez s/n, 33011 Oviedo, Spain.

We undertook a three-dimensional geometric morphometric (3DGM) analysis on 12 new Neandertal clavicle specimens from the El Sidrón site (Spain), dated to 49,000 years ago. The 3DGM methods were applied in a comparative framework in order to improve our understanding of trait polarity in features related to Homo pectoral girdle evolution, using other Neandertals, Homo sapiens, Pan, ATD6-50 (Homo antecessor), and KNM-WT 15000 (Homo ergaster/erectus) in the reference collection. Twenty-nine homologous landmarks were measured for each clavicle. Variation and morphological similarities were assessed through principal component analysis, conducted separately for the complete clavicle and the diaphysis. On average, Neandertal clavicles had significantly larger muscular entheses, double dorsal curvature, clavicle torsion, and cranial orientation of the acromial end than non-Neandertal clavicles; the El Sidrón clavicles fit this pattern. Variation within the samples was large, with extensive overlap between Homo species; only chimpanzee specimens clearly differed from the other specimens in morphometric terms. Taken together, our morphometric analyses are consistent with the following phylogenetic sequence. The primitive condition of the clavicle is manifest in the cranial orientation of both the acromial and sternal ends. The derived condition expressed in the H. sapiens + Neandertal clade is defined by caudal rotation of both the sternal and acromial ends, but with variation in the number of acromia remaining in a certain cranial orientation. Finally, the autapomorphic Neandertal condition is defined by secondarily acquired primitive cranial re-orientation of the acromial end, which varies from individual to individual. These results suggest that the pace of phylogenetic change in the pectoral girdle does not seem to follow that of other postcranial skeletal features.
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http://dx.doi.org/10.1016/j.jhevol.2016.03.005DOI Listing
June 2016

Ancient gene flow from early modern humans into Eastern Neanderthals.

Nature 2016 Feb 17;530(7591):429-33. Epub 2016 Feb 17.

Department of Evolutionary Genetics, Max Planck Institute for Evolutionary Anthropology, 04103 Leipzig, Germany.

It has been shown that Neanderthals contributed genetically to modern humans outside Africa 47,000-65,000 years ago. Here we analyse the genomes of a Neanderthal and a Denisovan from the Altai Mountains in Siberia together with the sequences of chromosome 21 of two Neanderthals from Spain and Croatia. We find that a population that diverged early from other modern humans in Africa contributed genetically to the ancestors of Neanderthals from the Altai Mountains roughly 100,000 years ago. By contrast, we do not detect such a genetic contribution in the Denisovan or the two European Neanderthals. We conclude that in addition to later interbreeding events, the ancestors of Neanderthals from the Altai Mountains and early modern humans met and interbred, possibly in the Near East, many thousands of years earlier than previously thought.
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http://dx.doi.org/10.1038/nature16544DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4933530PMC
February 2016

Possible Further Evidence of Low Genetic Diversity in the El Sidrón (Asturias, Spain) Neandertal Group: Congenital Clefts of the Atlas.

PLoS One 2015 29;10(9):e0136550. Epub 2015 Sep 29.

Área de Prehistoria, Department of History, Universidad de Oviedo, Oviedo, Spain.

We present here the first cases in Neandertals of congenital clefts of the arch of the atlas. Two atlases from El Sidrón, northern Spain, present respectively a defect of the posterior (frequency in extant modern human populations ranging from 0.73% to 3.84%), and anterior (frequency in extant modern human populations ranging from 0.087% to 0.1%) arch, a condition in most cases not associated with any clinical manifestation. The fact that two out of three observable atlases present a low frequency congenital condition, together with previously reported evidence of retained deciduous mandibular canine in two out of ten dentitions from El Sidrón, supports the previous observation based on genetic evidence that these Neandertals constituted a group with close genetic relations. Some have proposed for humans and other species that the presence of skeletal congenital conditions, although without clinical significance, could be used as a signal of endogamy or inbreeding. In the present case this interpretation would fit the general scenario of high incidence of rare conditions among Pleistocene humans and the specific scenariothat emerges from Neandertal paleogenetics, which points to long-term small and decreasing population size with reduced and isolated groups. Adverse environmental factors affecting early pregnancies would constitute an alternative, non-exclusive, explanation for a high incidence of congenital conditions. Further support or rejection of these interpretations will come from new genetic and skeletal evidence from Neandertal remains.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0136550PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4587856PMC
June 2016

A geometric morphometrics comparative analysis of Neandertal humeri (epiphyses-fused) from the El Sidrón cave site (Asturias, Spain).

J Hum Evol 2015 May 24;82:51-66. Epub 2015 Mar 24.

Área de Prehistoria, Department of History, Universidad de Oviedo, Calle Teniente Alfonso Martínez s/n, 33011 Oviedo, Spain.

A new collection of 49,000 year old Neandertal fossil humeri from the El Sidrón cave site (Asturias, Spain) is presented. A total of 49 humeral remains were recovered, representing 10 left and 8 right humeri from adults, adolescents, and a juvenile (not included in the analyses). 3D geometric morphometric (GM) methods as well as classic anthropological variables were employed to conduct a broad comparative analysis by means of mean centroid size and shape comparisons, principal components analysis, and cluster studies. Due to the fragmentary nature of the fossils, comparisons were organized in independent analyses according to different humeral portions: distal epiphysis, diaphysis, proximal epiphysis, and the complete humerus. From a multivariate viewpoint, 3D-GM analyses revealed major differences among taxonomic groups, supporting the value of the humerus in systematic classification. Notably, the Australopithecus anamensis (KP-271) and Homo ergaster Nariokotome (KNM-WT 15000) distal humerus consistently clusters close to those of modern humans, which may imply a primitive condition for Homo sapiens morphology. Australopithecus specimens show a high degree of dispersion in the morphospace. The El Sidrón sample perfectly fits into the classic Neandertal pattern, previously described as having a relatively wide olecranon fossa, as well as thin lateral and medial distodorsal pillars. These characteristics were also typical of the Sima de los Huesos (Atapuerca) sample, African mid-Pleistocene Bodo specimen, and Lower Pleistocene TD6-Atapuerca remains and may be considered as a derived state. Finally, we hypothesize that most of the features thought to be different between Neandertals and modern humans might be associated with structural differences in the pectoral girdle and shoulder joint.
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http://dx.doi.org/10.1016/j.jhevol.2015.02.018DOI Listing
May 2015

The relevance of the first ribs of the El Sidrón site (Asturias, Spain) for the understanding of the Neandertal thorax.

J Hum Evol 2015 Mar 3;80:64-73. Epub 2015 Jan 3.

Paleoanthropology Group, Museo Nacional de Ciencias Naturales (CSIC), J. G. Abascal 2, 28006, Madrid, Spain.

Reconstructing the morphology of the Neanderthal rib cage not only provides information about the general evolution of human body shape but also aids understanding of functional anatomy and energetics. Despite this paleobiological importance there is still debate about the nature and extent of variations in the size and shape of the Neandertal thorax. The El Sidrón Neandertals can be used to contribute to this debate, providing new costal remains ranging from fully preserved and undistorted ribs to highly fragmented elements. Six first ribs are particularly well preserved and offer the opportunity to analyze thorax morphology in Neandertals. The aims of this paper are to present this new material, to compare the ontogenetic trajectories of the first ribs between Neandertals and modern humans, and, using geometric morphometrics, to test the hypothesis of morphological integration between the first rib and overall thorax morphology. The first ribs of the El Sidrón adult Neandertals are smaller in centroid size and tend to be less curved when compared with those of modern humans, but are similar to Kebara 2. Our results further show that the straightening of the first ribs is significantly correlated with a straightening of the ribs of the upper thorax (R = 0.66; p < 0.0001) in modern humans, suggesting modularity in the upper and lower thorax units as reported in other hominins. It also supports the hypothesis that the upper thorax of Neandertals differs in shape from modern humans with more anteriorly projecting upper ribs during inspiration. These differences could have biomechanical consequences and account for stronger muscle attachments in Neandertals. Different upper thorax shape would also imply a different spatial arrangement of the shoulder girdle and articulation with the humerus (torsion) and its connection to the upper thorax. Future research should address these inferences in the context of Neandertal overall body morphology.
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http://dx.doi.org/10.1016/j.jhevol.2014.10.008DOI Listing
March 2015

The timing and spatiotemporal patterning of Neanderthal disappearance.

Nature 2014 Aug;512(7514):306-9

1] Department of Prehistory and Europe, Franks House, The British Museum, London N1 5QJ, UK [2] The Natural History Museum, Cromwell Road, London SW7 5BD, UK [3].

The timing of Neanderthal disappearance and the extent to which they overlapped with the earliest incoming anatomically modern humans (AMHs) in Eurasia are key questions in palaeoanthropology. Determining the spatiotemporal relationship between the two populations is crucial if we are to understand the processes, timing and reasons leading to the disappearance of Neanderthals and the likelihood of cultural and genetic exchange. Serious technical challenges, however, have hindered reliable dating of the period, as the radiocarbon method reaches its limit at ∼50,000 years ago. Here we apply improved accelerator mass spectrometry (14)C techniques to construct robust chronologies from 40 key Mousterian and Neanderthal archaeological sites, ranging from Russia to Spain. Bayesian age modelling was used to generate probability distribution functions to determine the latest appearance date. We show that the Mousterian ended by 41,030-39,260 calibrated years bp (at 95.4% probability) across Europe. We also demonstrate that succeeding 'transitional' archaeological industries, one of which has been linked with Neanderthals (Châtelperronian), end at a similar time. Our data indicate that the disappearance of Neanderthals occurred at different times in different regions. Comparing the data with results obtained from the earliest dated AMH sites in Europe, associated with the Uluzzian technocomplex, allows us to quantify the temporal overlap between the two human groups. The results reveal a significant overlap of 2,600-5,400 years (at 95.4% probability). This has important implications for models seeking to explain the cultural, technological and biological elements involved in the replacement of Neanderthals by AMHs. A mosaic of populations in Europe during the Middle to Upper Palaeolithic transition suggests that there was ample time for the transmission of cultural and symbolic behaviours, as well as possible genetic exchanges, between the two groups.
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http://dx.doi.org/10.1038/nature13621DOI Listing
August 2014

Temporal lobe sulcal pattern and the bony impressions in the middle cranial fossa: the case of the el Sidrón (Spain) neandertal sample.

Anat Rec (Hoboken) 2014 Dec 19;297(12):2331-41. Epub 2014 Jun 19.

Department of Paleobiology, Paleoanthropology Group MNCN-CSIC, Museo Nacional de Ciencias Naturales-CSIC, Calle José Gutiérrez Abascal 2, 28006, Madrid, Spain.

Correspondence between temporal lobe sulcal pattern and bony impressions on the middle cranial fossae (MCF) was analyzed. MCF bone remains (SD-359, SD-315, and SD-1219) from the El Sidrón (Spain) neandertal site are analyzed in this context. Direct comparison of the soft and hard tissues from the same individual was studied by means of: 1) dissection of two human heads; 2) optic (white light) surface scans; 3) computed tomography and magnetic resonance of the same head. The inferior temporal sulcus and gyrus are the features most strongly influencing MCF bone surface. The Superior temporal sulcus and middle temporal and fusiform gyri also leave imprints. Temporal lobe form differs between Homo sapiens and neandertals. A wider and larger post-arcuate fossa (posterior limit of Brodmann area 20 and the anterior portion of area 37) is present in modern humans as compared to neandertals. However other traits of the MCF surface are similar in these two large-brained human groups. A conspicuous variation is appreciated in the more vertical location of the inferior temporal gyrus in H. sapiens. In parallel, structures of the lower surface of the temporal lobe are more sagittally orientated. Grooves accommodating the fusiform and the lower temporal sulci become grossly parallel to the temporal squama. These differences can be understood within the context of a supero-lateral deployment of the lobe in H. sapiens, a pattern previously identified (Bastir et al., Nat Commun 2 (2011) 588-595). Regarding dural sinus pattern, a higher incidence of petrosquamous sinus is detected in neandertal samples.
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http://dx.doi.org/10.1002/ar.22957DOI Listing
December 2014

Patterns of coding variation in the complete exomes of three Neandertals.

Proc Natl Acad Sci U S A 2014 May 21;111(18):6666-71. Epub 2014 Apr 21.

Department of Evolutionary Genetics, Max Planck Institute for Evolutionary Anthropology, 04103 Leipzig, Germany.

We present the DNA sequence of 17,367 protein-coding genes in two Neandertals from Spain and Croatia and analyze them together with the genome sequence recently determined from a Neandertal from southern Siberia. Comparisons with present-day humans from Africa, Europe, and Asia reveal that genetic diversity among Neandertals was remarkably low, and that they carried a higher proportion of amino acid-changing (nonsynonymous) alleles inferred to alter protein structure or function than present-day humans. Thus, Neandertals across Eurasia had a smaller long-term effective population than present-day humans. We also identify amino acid substitutions in Neandertals and present-day humans that may underlie phenotypic differences between the two groups. We find that genes involved in skeletal morphology have changed more in the lineage leading to Neandertals than in the ancestral lineage common to archaic and modern humans, whereas genes involved in behavior and pigmentation have changed more on the modern human lineage.
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http://dx.doi.org/10.1073/pnas.1405138111DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4020111PMC
May 2014

Extreme population differences in the human zinc transporter ZIP4 (SLC39A4) are explained by positive selection in Sub-Saharan Africa.

PLoS Genet 2014 Feb 20;10(2):e1004128. Epub 2014 Feb 20.

Institute of Evolutionary Biology (CSIC-UPF), Department of Experimental and Health Sciences, Universitat Pompeu Fabra, Barcelona, Spain.

Extreme differences in allele frequency between West Africans and Eurasians were observed for a leucine-to-valine substitution (Leu372Val) in the human intestinal zinc uptake transporter, ZIP4, yet no further evidence was found for a selective sweep around the ZIP4 gene (SLC39A4). By interrogating allele frequencies in more than 100 diverse human populations and resequencing Neanderthal DNA, we confirmed the ancestral state of this locus and found a strong geographical gradient for the derived allele (Val372), with near fixation in West Africa. In extensive coalescent simulations, we show that the extreme differences in allele frequency, yet absence of a classical sweep signature, can be explained by the effect of a local recombination hotspot, together with directional selection favoring the Val372 allele in Sub-Saharan Africans. The possible functional effect of the Leu372Val substitution, together with two pathological mutations at the same codon (Leu372Pro and Leu372Arg) that cause acrodermatitis enteropathica (a disease phenotype characterized by extreme zinc deficiency), was investigated by transient overexpression of human ZIP4 protein in HeLa cells. Both acrodermatitis mutations cause absence of the ZIP4 transporter cell surface expression and nearly absent zinc uptake, while the Val372 variant displayed significantly reduced surface protein expression, reduced basal levels of intracellular zinc, and reduced zinc uptake in comparison with the Leu372 variant. We speculate that reduced zinc uptake by the ZIP4-derived Val372 isoform may act by starving certain pathogens of zinc, and hence may have been advantageous in Sub-Saharan Africa. Moreover, these functional results may indicate differences in zinc homeostasis among modern human populations with possible relevance for disease risk.
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http://dx.doi.org/10.1371/journal.pgen.1004128DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3930504PMC
February 2014

A recent evolutionary change affects a regulatory element in the human FOXP2 gene.

Mol Biol Evol 2013 Apr 28;30(4):844-52. Epub 2012 Nov 28.

Department of Evolutionary Genetics, Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany.

The FOXP2 gene is required for normal development of speech and language. By isolating and sequencing FOXP2 genomic DNA fragments from a 49,000-year-old Iberian Neandertal and 50 present-day humans, we have identified substitutions in the gene shared by all or nearly all present-day humans but absent or polymorphic in Neandertals. One such substitution is localized in intron 8 and affects a binding site for the transcription factor POU3F2, which is highly conserved among vertebrates. We find that the derived allele of this site is less efficient than the ancestral allele in activating transcription from a reporter construct. The derived allele also binds less POU3F2 dimers than POU3F2 monomers compared with the ancestral allele. Because the substitution in the POU3F2 binding site is likely to alter the regulation of FOXP2 expression, and because it is localized in a region of the gene associated with a previously described signal of positive selection, it is a plausible candidate for having caused a recent selective sweep in the FOXP2 gene.
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http://dx.doi.org/10.1093/molbev/mss271DOI Listing
April 2013

Neanderthal medics? Evidence for food, cooking, and medicinal plants entrapped in dental calculus.

Naturwissenschaften 2012 Aug 18;99(8):617-26. Epub 2012 Jul 18.

ICREA at Universitat Autònoma de Barcelona, Barcelona, Spain.

Neanderthals disappeared sometime between 30,000 and 24,000 years ago. Until recently, Neanderthals were understood to have been predominantly meat-eaters; however, a growing body of evidence suggests their diet also included plants. We present the results of a study, in which sequential thermal desorption-gas chromatography-mass spectrometry (TD-GC-MS) and pyrolysis-gas chromatography-mass spectrometry (Py-GC-MS) were combined with morphological analysis of plant microfossils, to identify material entrapped in dental calculus from five Neanderthal individuals from the north Spanish site of El Sidrón. Our results provide the first molecular evidence for inhalation of wood-fire smoke and bitumen or oil shale and ingestion of a range of cooked plant foods. We also offer the first evidence for the use of medicinal plants by a Neanderthal individual. The varied use of plants that we have identified suggests that the Neanderthal occupants of El Sidrón had a sophisticated knowledge of their natural surroundings which included the ability to select and use certain plants.
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http://dx.doi.org/10.1007/s00114-012-0942-0DOI Listing
August 2012

Analysis of human accelerated DNA regions using archaic hominin genomes.

PLoS One 2012 7;7(3):e32877. Epub 2012 Mar 7.

Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany.

Several previous comparisons of the human genome with other primate and vertebrate genomes identified genomic regions that are highly conserved in vertebrate evolution but fast-evolving on the human lineage. These human accelerated regions (HARs) may be regions of past adaptive evolution in humans. Alternatively, they may be the result of non-adaptive processes, such as biased gene conversion. We captured and sequenced DNA from a collection of previously published HARs using DNA from an Iberian Neandertal. Combining these new data with shotgun sequence from the Neandertal and Denisova draft genomes, we determine at least one archaic hominin allele for 84% of all positions within HARs. We find that 8% of HAR substitutions are not observed in the archaic hominins and are thus recent in the sense that the derived allele had not come to fixation in the common ancestor of modern humans and archaic hominins. Further, we find that recent substitutions in HARs tend to have come to fixation faster than substitutions elsewhere in the genome and that substitutions in HARs tend to cluster in time, consistent with an episodic rather than a clock-like process underlying HAR evolution. Our catalog of sequence changes in HARs will help prioritize them for functional studies of genomic elements potentially responsible for modern human adaptations.
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http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0032877PLOS
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3296746PMC
August 2012

An ancestral miR-1304 allele present in Neanderthals regulates genes involved in enamel formation and could explain dental differences with modern humans.

Mol Biol Evol 2012 Jul 27;29(7):1797-806. Epub 2012 Jan 27.

Institut de Biologia Evolutiva, Universitat Pompeu Fabra-Consejo Superior de Investigaciones Científicas, Barcelona, Catalonia, Spain.

Genetic changes in regulatory elements are likely to result in phenotypic effects that might explain population-specific as well as species-specific traits. MicroRNAs (miRNAs) are posttranscriptional repressors involved in the control of almost every biological process. These small noncoding RNAs are present in various phylogenetic groups, and a large number of them remain highly conserved at the sequence level. MicroRNA-mediated regulation depends on perfect matching between the seven nucleotides of its seed region and the target sequence usually located at the 3' untranslated region of the regulated gene. Hence, even single changes in seed regions are predicted to be deleterious as they may affect miRNA target specificity. In accordance to this, purifying selection has strongly acted on these regions. Comparison between the genomes of present-day humans from various populations, Neanderthal, and other nonhuman primates showed an miRNA, miR-1304, that carries a polymorphism on its seed region. The ancestral allele is found in Neanderthal, nonhuman primates, at low frequency (~5%) in modern Asian populations and rarely in Africans. Using miRNA target site prediction algorithms, we found that the derived allele increases the number of putative target genes for the derived miRNA more than ten-fold, indicating an important functional evolution for miR-1304. Analysis of the predicted targets for derived miR-1304 indicates an association with behavior and nervous system development and function. Two of the predicted target genes for the ancestral miR-1304 allele are important genes for teeth formation, enamelin, and amelotin. MicroRNA overexpression experiments using a luciferase-based assay showed that the ancestral version of miR-1304 reduces the enamelin- and amelotin-associated reporter gene expression by 50%, whereas the derived miR-1304 does not have any effect. Deletion of the corresponding target sites for miR-1304 in these dental genes avoided their repression, which further supports their regulation by the ancestral miR-1304. Morphological studies described several differences in the dentition of Neanderthals and present-day humans like slower dentition timing and thicker enamel for present-day humans. The observed miR-1304-mediated regulation of enamelin and amelotin could at least partially underlie these differences between the two Homo species as well as other still-unraveled phenotypic differences among modern human populations.
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http://dx.doi.org/10.1093/molbev/mss023DOI Listing
July 2012

Paleoneurology of two new neandertal occipitals from El Sidrón (asturias, Spain) in the context of homo endocranial evolution.

Anat Rec (Hoboken) 2011 Aug 28;294(8):1370-81. Epub 2011 Jun 28.

Departamento de Anatomía y Embriología Humana I, Facultad de Medicina, Universidad Complutense de Madrid, Spain.

The endocranial surface description and comparative analyses of two new neandertal occipital fragments (labelled SD-1149 and SD-370a) from the El Sidrón site (Asturias, Spain) reveal new aspects of neandertal brain morphological asymmetries. The dural sinus drainage pattern, as observed on the sagittal-transverse system, as well as the cerebral occipito-petalias, point out a slightly differential configuration of the neandertal brain when compared to other Homo species, especially H. sapiens. The neandertal dural sinus drainage pattern is organized in a more asymmetric mode, in such a way that the superior sagittal sinus (SSS) drains either to the right or to the left transverse sinuses, but in no case in a confluent mode (i.e. simultaneous continuation of SSS with both right (RTS) and left (LTS) transverse sinuses). Besides, the superior sagittal sinus shows an accentuated deviation from of the mid-sagittal plane in its way to the RTS in 35% of neandertals. This condition, which increases the asymmetry of the system, is almost nonexistent neither in the analyzed Homo fossil species sample nor in that of anatomically modern humans. Regarding the cerebral occipito-petalias, neandertals manifest one of the lowest percentages of left petalia of the Homo sample (including modern H. sapiens). As left occipito-petalia is the predominant pattern in hominins, it seems as if neandertals would have developed a different pattern of brain hemispheres asymmetry. Finally, the relief and position of the the cerebral sulci and gyri impressions observed in the El Sidrón occipital specimens look similar to those observed in modern H. sapiens.
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http://dx.doi.org/10.1002/ar.21427DOI Listing
August 2011

Palaeogenetic research at the El Sidrón Neanderthal site.

Ann Anat 2012 Jan 17;194(1):133-7. Epub 2011 Mar 17.

Institute of Evolutionary Biology, Barcelona, Spain.

El Sidrón (Asturias, north of Spain) is a subterranean karstic system, where the remains of a contemporaneous social Neanderthal group dated to about 49,000 years ago have been being excavated since their accidental discovery in 1994. Due to the particular preservation conditions of this site, all individuals identified so far have preserved DNA, and the anticontamination measures implemented during the excavation have made palaeogenetic studies possible on all individuals. The El Sidrón samples provide unique information on the kinship relationships and on the internal genetic diversity of Neanderthal groups, thus yielding for first time empirical data for the generation of demographic models of these extinct humans. Moreover, the exceptional preservation of some bone samples has allowed the retrieval of nuclear genes associated with some phenotypic traits involved in pigmentation, blood group, language or taste perception, as well as a significant fraction (0.1%) of the nuclear genome. A future project on Neanderthal genomic diversity could be based on at least some of the El Sidrón specimens.
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http://dx.doi.org/10.1016/j.aanat.2011.01.014DOI Listing
January 2012

Bone remodelling in Neanderthal mandibles from the El Sidrón site (Asturias, Spain).

Biol Lett 2011 Aug 9;7(4):593-6. Epub 2011 Feb 9.

ISTeP, UPMC University Paris 6, UMR 7193, 75005 Paris, France.

Skull morphology results from the bone remodelling mechanism that underlies the specific bone growth dynamics. Histological study of the bone surface from Neanderthal mandible specimens of El Sidrón (Spain) provides information about the distribution of the remodelling fields (bone remodelling patterns or BRP) indicative of the bone growth directions. In comparison with other primate species, BRP shows that Neanderthal mandibles from the El Sidrón (Spain) sample present a specific BRP. The interpretation of this map allows inferences concerning the growth directions that explain specific morphological traits of the Neanderthal mandible, such as its quadrangular shape and the posterior location of the mental foramen.
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http://dx.doi.org/10.1098/rsbl.2010.1188DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3130222PMC
August 2011

Genetic evidence for patrilocal mating behavior among Neandertal groups.

Proc Natl Acad Sci U S A 2011 Jan 20;108(1):250-3. Epub 2010 Dec 20.

Institute of Evolutionary Biology, Consejo Superior de Investigaciones Cientificas-Universitat Pompeu Fabra, 08003 Barcelona, Spain.

The remains of 12 Neandertal individuals have been found at the El Sidrón site (Asturias, Spain), consisting of six adults, three adolescents, two juveniles, and one infant. Archaeological, paleontological, and geological evidence indicates that these individuals represent all or part of a contemporaneous social group of Neandertals, who died at around the same time and later were buried together as a result of a collapse of an underground karst. We sequenced phylogenetically informative positions of mtDNA hypervariable regions 1 and 2 from each of the remains. Our results show that the 12 individuals stem from three different maternal lineages, accounting for seven, four, and one individual(s), respectively. Using a Y-chromosome assay to confirm the morphological determination of sex for each individual, we found that, although the three adult males carried the same mtDNA lineage, each of the three adult females carried different mtDNA lineages. These findings provide evidence to indicate that Neandertal groups not only were small and characterized by low genetic diversity but also were likely to have practiced patrilocal mating behavior.
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http://dx.doi.org/10.1073/pnas.1011553108DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3017130PMC
January 2011

Brief communication: Subvertical grooves on interproximal wear facets from the El Sidrón (Asturias, Spain) Neandertal dental sample.

Am J Phys Anthropol 2011 Jan;144(1):154-61

PaleoAnthropology Group, Department of Paleobiology, Museo Nacional de Ciencias Naturales, CSIC, Calle José Gutiérrez Abascal 2, Madrid, Spain.

The distribution of subvertical grooves on interproximal wear dental facets from the El Sidrón (Asturias, Spain) Neandertals is described and analyzed. Out of 93 teeth, 64.5% present subvertical grooves, including a high frequency (50%) on the anterior dentition. Contrary to some studies, subvertical grooves from adjacent facets perfectly overlap each other and do not interdigitate, probably forming small channels. Both the facet and the groove surface share the same polished appearance, suggesting a common origin. Statistical analyses reveal that the number of grooves is neither dependent on the degree of occlusal wear, nor on the position on the tooth or the individual's age. However, facet width is an important factor determining the number of subvertical grooves. The etiology of subvertical grooves formation on Neandertal teeth remains unclear.
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http://dx.doi.org/10.1002/ajpa.21359DOI Listing
January 2011