Dairying, diseases and the evolution of lactase persistence in Europe.

In European and many African, Middle Eastern and southern Asian populations, lactase persistence (LP) is the most strongly selected monogenic trait to have evolved over the past 10,000 years1. Although the selection of LP and the consumption of prehistoric milk must be linked, considerable uncertainty remains concerning their spatiotemporal configuration and specific interactions2,3. Here we provide detailed distributions of milk exploitation across Europe over the past 9,000 years using around 7,000 pottery fat residues from more than 550 archaeological sites. European milk use was widespread from the Neolithic period onwards but varied spatially and temporally in intensity. Notably, LP selection varying with levels of prehistoric milk exploitation is no better at explaining LP allele frequency trajectories than uniform selection since the Neolithic period. In the UK Biobank4,5 cohort of 500,000 contemporary Europeans, LP genotype was only weakly associated with milk consumption and did not show consistent associations with improved fitness or health indicators. This suggests that other reasons for the beneficial effects of LP should be considered for its rapid frequency increase. We propose that lactase non-persistent individuals consumed milk when it became available but, under conditions of famine and/or increased pathogen exposure, this was disadvantageous, driving LP selection in prehistoric Europe. Comparison of model likelihoods indicates that population fluctuations, settlement density and wild animal exploitation-proxies for these drivers-provide better explanations of LP selection than the extent of milk exploitation. These findings offer new perspectives on prehistoric milk exploitation and LP evolution.

Ancient pigs reveal a near-complete genomic turnover following their introduction to Europe.

Archaeological evidence indicates that pig domestication had begun by ∼10,500 y before the present (BP) in the Near East, and mitochondrial DNA (mtDNA) suggests that pigs arrived in Europe alongside farmers ∼8,500 y BP. A few thousand years after the introduction of Near Eastern pigs into Europe, however, their characteristic mtDNA signature disappeared and was replaced by haplotypes associated with European wild boars. This turnover could be accounted for by substantial gene flow from local European wild boars, although it is also possible that European wild boars were domesticated independently without any genetic contribution from the Near East. To test these hypotheses, we obtained mtDNA sequences from 2,099 modern and ancient pig samples and 63 nuclear ancient genomes from Near Eastern and European pigs. Our analyses revealed that European domestic pigs dating from 7,100 to 6,000 y BP possessed both Near Eastern and European nuclear ancestry, while later pigs possessed no more than 4% Near Eastern ancestry, indicating that gene flow from European wild boars resulted in a near-complete disappearance of Near East ancestry. In addition, we demonstrate that a variant at a locus encoding black coat color likely originated in the Near East and persisted in European pigs. Altogether, our results indicate that while pigs were not independently domesticated in Europe, the vast majority of human-mediated selection over the past 5,000 y focused on the genomic fraction derived from the European wild boars, and not on the fraction that was selected by early Neolithic farmers over the first 2,500 y of the domestication process.

Four millennia of Iberian biomolecular prehistory illustrate the impact of prehistoric migrations at the far end of Eurasia.

Population genomic studies of ancient human remains have shown how modern-day European population structure has been shaped by a number of prehistoric migrations. The Neolithization of Europe has been associated with large-scale migrations from Anatolia, which was followed by migrations of herders from the Pontic steppe at the onset of the Bronze Age. Southwestern Europe was one of the last parts of the continent reached by these migrations, and modern-day populations from this region show intriguing similarities to the initial Neolithic migrants. Partly due to climatic conditions that are unfavorable for DNA preservation, regional studies on the Mediterranean remain challenging. Here, we present genome-wide sequence data from 13 individuals combined with stable isotope analysis from the north and south of Iberia covering a four-millennial temporal transect (7,500-3,500 BP). Early Iberian farmers and Early Central European farmers exhibit significant genetic differences, suggesting two independent fronts of the Neolithic expansion. The first Neolithic migrants that arrived in Iberia had low levels of genetic diversity, potentially reflecting a small number of individuals; this diversity gradually increased over time from mixing with local hunter-gatherers and potential population expansion. The impact of post-Neolithic migrations on Iberia was much smaller than for the rest of the continent, showing little external influence from the Neolithic to the Bronze Age. Paleodietary reconstruction shows that these populations have a remarkable degree of dietary homogeneity across space and time, suggesting a strong reliance on terrestrial food resources despite changing culture and genetic make-up.

Exploring bone volume and skeletal weight in the Middle Pleistocene humans from the Sima de los Huesos site (Sierra de Atapuerca, Spain).

Body mass estimation in fossil human species is a crucial topic in paleoanthropology as it yields information about ecologically relevant characteristics. Nevertheless, variables crucial to body mass estimation such as bone volume and skeletal weight have never before been calculated in a fossil human species. The exceptional state of preservation of several fossil human long bones from the Sima de los Huesos (SH) Middle Pleistocene site, in the Sierra de Atapuerca, makes it possible to calculate for the first time the absolute bone volume in five complete long bones (two femora and three humeri) of a fossil human species, an approach not possible in fragmentary or poorly preserved fossils. We have relied on computed tomography scans and 3D reconstructions to calculate bone volume. A sample of 62 complete bones of robust recent humans was also used for comparative purposes. The male SH femora (weight-bearing bones) and humeri (non-weight-bearing bones) have, relative to their size, greater bone volume (volume of bone tissue over total bone volume) than the equivalent bones in our recent human sample. As mass is volume × density, and bone tissue density (as a material) is similar across mammals, we calculate bone mass, and our results show that the SH hominins had on average heavier long bones than extant humans of the same size. From the femoral weight at hand, we have estimated the total skeletal weight in two SH individuals, which is about 36% heavier than in the recent humans of the equivalent body size. Using different methods and skeletal variables, including skeletal weight, to estimate body mass in these two SH humans, we highlight the considerable differences in body mass estimates we obtained, and that the largest body mass estimate is the one based on the skeletal weight. Our results suggest that we cannot assume the same relative proportion of bone volume and bone and skeletal weight characterized the entire genus Homo. Given that skeletal weight has a significant influence on body mass, current body mass estimates of fossil Homo specimens could be systematically underestimated. Thus, the significantly larger bone volume and heavier bones, probably throughout the entire skeleton, of SH humans could have had consequences for many biological parameters in this Pleistocene population and considerable importance for studies focusing on adaptive and ecologically relevant characteristics. Although more recent human samples should be analyzed, in our view, the high skeletal robusticity of the SH sample, including larger bone volume and skeletal weight, is part of their adaptive body type selected for throughout the Pleistocene to support different mechanical and activity regimes and formed under tight genetic control, including control over bone formative and regulatory processes.

Cross-sectional properties of the lower limb long bones in the Middle Pleistocene Sima de los Huesos sample (Sierra de Atapuerca, Spain).

The recovery to date of three complete and five partial femora, seven complete tibiae, and four complete fibulae from the Atapuerca Sima de los Huesos site provides an opportunity to analyze the biomechanical cross-sectional properties in this Middle Pleistocene population and to compare them with those of other fossil hominins and recent modern humans. We have performed direct comparisons of the cross-sectional geometric parameters and reduced major axis (RMA) regression lines among different samples. We have determined that Atapuerca Sima de los Huesos (SH) fossils have significantly thicker cortices than those of recent modern humans for the three leg bones at all diaphyseal levels, except that of the femur at 35% of biomechanical length. The SH bones are similar to those of Neandertals and Middle Pleistocene humans and different from Homo sapiens in their diaphyseal cross-sectional shape and strength parameters. When standardized by estimated body size, both the SH and Neandertal leg bones have in general greater strength than those of H. sapiens from the early modern (EMH), Upper Paleolithic (UP), and recent populations (RH). The Sima de los Huesos human leg bones have, in general terms, an ancestral pattern similar to that of Pleistocene humans and differing from H. sapiens.

Postcranial morphology of the middle Pleistocene humans from Sima de los Huesos, Spain.

Current knowledge of the evolution of the postcranial skeleton in the genus Homo is hampered by a geographically and chronologically scattered fossil record. Here we present a complete characterization of the postcranium of the middle Pleistocene paleodeme from the Sima de los Huesos (SH) and its paleobiological implications. The SH hominins show the following: (i) wide bodies, a plesiomorphic character in the genus Homo inherited from their early hominin ancestors; (ii) statures that can be found in modern human middle-latitude populations that first appeared 1.6-1.5 Mya; and (iii) large femoral heads in some individuals, a trait that first appeared during the middle Pleistocene in Africa and Europe. The intrapopulational size variation in SH shows that the level of dimorphism was similar to modern humans (MH), but the SH hominins were less encephalized than Neandertals. SH shares many postcranial anatomical features with Neandertals. Although most of these features appear to be either plesiomorphic retentions or are of uncertain phylogenetic polarity, a few represent Neandertal apomorphies. Nevertheless, the full suite of Neandertal-derived features is not yet present in the SH population. The postcranial evidence is consistent with the hypothesis based on the cranial morphology that the SH hominins are a sister group to the later Neandertals. Comparison of the SH postcranial skeleton to other hominins suggests that the evolution of the postcranium occurred in a mosaic mode, both at a general and at a detailed level.

Ancient genomes link early farmers from Atapuerca in Spain to modern-day Basques.

The consequences of the Neolithic transition in Europe--one of the most important cultural changes in human prehistory--is a subject of great interest. However, its effect on prehistoric and modern-day people in Iberia, the westernmost frontier of the European continent, remains unresolved. We present, to our knowledge, the first genome-wide sequence data from eight human remains, dated to between 5,500 and 3,500 years before present, excavated in the El Portalón cave at Sierra de Atapuerca, Spain. We show that these individuals emerged from the same ancestral gene pool as early farmers in other parts of Europe, suggesting that migration was the dominant mode of transferring farming practices throughout western Eurasia. In contrast to central and northern early European farmers, the Chalcolithic El Portalón individuals additionally mixed with local southwestern hunter-gatherers. The proportion of hunter-gatherer-related admixture into early farmers also increased over the course of two millennia. The Chalcolithic El Portalón individuals showed greatest genetic affinity to modern-day Basques, who have long been considered linguistic and genetic isolates linked to the Mesolithic whereas all other European early farmers show greater genetic similarity to modern-day Sardinians. These genetic links suggest that Basques and their language may be linked with the spread of agriculture during the Neolithic. Furthermore, all modern-day Iberian groups except the Basques display distinct admixture with Caucasus/Central Asian and North African groups, possibly related to historical migration events. The El Portalón genomes uncover important pieces of the demographic history of Iberia and Europe and reveal how prehistoric groups relate to modern-day people.

Fossil hominin radii from the Sima de los Huesos Middle Pleistocene site (Sierra de Atapuerca, Spain).

Complete radii in the fossil record preceding recent humans and Neandertals are very scarce. Here we introduce the radial remains recovered from the Sima de los Huesos (SH) site in the Sierra de Atapuerca between 1976 and 2011 and which have been dated in excess of 430 ky (thousands of years) ago. The sample comprises 89 specimens, 49 of which are attributed to adults representing a minimum of seven individuals. All elements are described anatomically and metrically, and compared with other fossil hominins and recent humans in order to examine the phylogenetic polarity of certain radial features. Radial remains from SH have some traits that differentiate them from those of recent humans and make them more similar to Neandertals, including strongly curved shafts, anteroposterior expanded radial heads and both absolutely and relatively long necks. In contrast, the SH sample differs from Neandertals in showing a high overall gracility as well as a high frequency (80%) of an anteriorly oriented radial tuberosity. Thus, like the cranial and dental remains from the SH site, characteristic Neandertal radial morphology is not present fully in the SH radii. We also analyzed the cross-sectional properties of the SH radial sample at two different levels: mid-shaft and at the midpoint of the neck length. When standardized by shaft length, no difference in the mid-shaft cross-sectional properties were found between the SH hominins, Neandertals and recent humans. Nevertheless, due to their long neck length, the SH hominins show a higher lever efficiency than either Neandertals or recent humans. Functionally, the SH radial morphology is consistent with more efficient pronation-supination and flexion-extension movements. The particular trait composition in the SH sample and Neandertals resembles more closely morphology evident in recent human males.

Virtual reconstruction of the Early Pleistocene mandible ATD6-96 from Gran Dolina-TD6-2 (Sierra De Atapuerca, Spain).

OBJECTIVES: In this report, we present a further study of the late Early Pleistocene ATD6-96 human mandible, recovered from the TD6-2 level of the Gran Dolina cave site (Sierra de Atapuerca, northern Spain) and attributed to Homo antecessor. METHODS: ATD6-96 consists of a left half of a gracile mandible of an adult individual with the premolars and molars in place that is broken at the level of the lateral incisor-canine septum. The present analysis is based on a virtual reconstruction of the whole mandible by means of computed tomography (CT). We have reconstructed the symphysis using information from a modern human sample, as well as from a wide sample composed of several Homo specimens. RESULTS: This research has allowed us to record new variables with taxonomic and phylogenetic interest. We have estimated the length/width index of the alveolar arcade, as well as the percentage of the arcade length with regard to the total length. The latter confirms that ATD6-96 shares with all African and Asian Homo species a primitive structural pattern, as it was established in previous studies. In constrast, the length/width index of the alveolar arcade in the H. antecessor specimen is close to the mean values of Neandertals and the Atapuerca-Sima de los Huesos hominins. CONCLUSIONS: H. antecessor is derived regarding the shape of the mandibular alveolar arcade within the genus Homo and points to an early divergence from contemporaneous African populations. Our results also ratify the affinities of H. antecessor with Neanderthals, although the precise relationship with this lineage needs further research.

Direct estimates of natural selection in Iberia indicate calcium absorption was not the only driver of lactase persistence in Europe.

Lactase persistence (LP) is a genetically determined trait whereby the enzyme lactase is expressed throughout adult life. Lactase is necessary for the digestion of lactose--the main carbohydrate in milk--and its production is downregulated after the weaning period in most humans and all other mammals studied. Several sources of evidence indicate that LP has evolved independently, in different parts of the world over the last 10,000 years, and has been subject to strong natural selection in dairying populations. In Europeans, LP is strongly associated with, and probably caused by, a single C to T mutation 13,910 bp upstream of the lactase (LCT) gene (-13,910*T). Despite a considerable body of research, the reasons why LP should provide such a strong selective advantage remain poorly understood. In this study, we examine one of the most widely cited hypotheses for selection on LP--that fresh milk consumption supplemented the poor vitamin D and calcium status of northern Europe's early farmers (the calcium assimilation hypothesis). We do this by testing for natural selection on -13,910*T using ancient DNA data from the skeletal remains of eight late Neolithic Iberian individuals, whom we would not expect to have poor vitamin D and calcium status because of relatively high incident UVB light levels. None of the eight samples successfully typed in the study had the derived T-allele. In addition, we reanalyze published data from French Neolithic remains to both test for population continuity and further examine the evolution of LP in the region. Using simulations that accommodate genetic drift, natural selection, uncertainty in calibrated radiocarbon dates, and sampling error, we find that natural selection is still required to explain the observed increase in allele frequency. We conclude that the calcium assimilation hypothesis is insufficient to explain the spread of LP in Europe.

Early Pleistocene human hand phalanx from the Sima del Elefante (TE) cave site in Sierra de Atapuerca (Spain).

In this study, a new Early Pleistocene proximal hand phalanx (ATE9-2) from the Sima del Elefante cave site (TE - Sierra de Atapuerca, Spain), ascribed to Homo sp., is presented and comparatively described in the context of the evolution of the genus Homo. The ATE9-2 specimen is especially important because of the paucity of hand bones in the human fossil record during the Early Pleistocene. The morphological and metrical analyses of the phalanx ATE9-2 indicate that there are no essential differences between it and comparator fossil specimens for the genus Homo after 1.3 Ma (millions of years ago). Similar to Sima de los Huesos and Neandertal specimens, ATE9-2 is a robust proximal hand phalanx, probably reflecting greater overall body robusticity in these populations or a higher gracility in modern humans. The age of level TE9 from Sima del Elefante and morphological and metrical studies of ATE9-2 suggest that the morphology of the proximal hand phalanges and, thus, the morphology of the hand could have remained stable over the last 1.2-1.3 Ma. Taking into account the evidence recently provided by a metacarpal from Kaitio (Kenya) from around 1.42 Ma, we argue that modern hand morphology is present in the genus Homo subsequent to Homo habilis.

How the Sima de los Huesos was won.

Although the first discovery of a human fossil in the Sima de los Huesos took place in 1976, systematic excavations did not begin there until 1984. Since then, this site has been continuously excavated in month-long camps. The site is dated by different radiometric techniques to between 430,000 and 300,000 years ago. Until the 2023 campaign, just over 7000 human fossils have been recovered, constituting the largest collection of fossils prior to Homo sapiens ever discovered. The fossils correspond to a minimum of 29 individuals of both sexes and different ages at death, from preadolescents to a specimen of advanced age. Comparative anatomy and ancient DNA studies both suggest that this is a population closely related to Homo neanderthalensis. The great variety and extraordinary quality of the fossils recovered have allowed us to carry out a series of investigations that have greatly increased our knowledge about the evolution of Homo in the Middle Pleistocene. Among the most important discoveries, it has been possible to establish body size and proportions, the confirmation that the origin of the accumulation of human fossils was of an anthropic nature, that those past humans took care of disabled individuals and who were capable of having an oral language almost as complex and efficient as that of our own species.

The child who lived: Down syndrome among Neanderthals?

Caregiving for disabled individuals among Neanderthals has been known for a long time, and there is a debate about the implications of this behavior. Some authors believe that caregiving took place between individuals able to reciprocate the favor, while others argue that caregiving was produced by a feeling of compassion related to other highly adaptive prosocial behaviors. The study of children with severe pathologies is particularly interesting, as children have a very limited possibility to reciprocate the assistance. We present the case of a Neanderthal child who suffered from a congenital pathology of the inner ear, probably debilitating, and associated with Down syndrome. This child would have required care for at least 6 years, likely necessitating other group members to assist the mother in childcare.

Middle Pleistocene lower back and pelvis from an aged human individual from the Sima de los Huesos site, Spain.

We report a nearly complete lumbar spine from the Middle Pleistocene site of the Sima de los Huesos (SH) that is assigned to the previously published SH male Pelvis 1 [Arsuaga JL, et al. (1999). Nature 399: 255-258]. The "SH Pelvis 1 individual" is a unique nearly complete lumbo-pelvic complex from the human Middle Pleistocene fossil record, and offers a rare glimpse into the anatomy and past lifeways of Homo heidelbergensis. A revised reconstruction of Pelvis 1, together with the current fossil evidence, confirms our previous hypothesis that the morphology of this pelvis represents the primitive pattern within the genus Homo. Here we argue that this primitive pattern is also characterized by sexual dimorphism in the pelvic canal shape, implying complicated deliveries. In addition, this individual shows signs of lumbar kyphotic deformity, spondylolisthesis, and Baastrup disease. This suite of lesions would have postural consequences and was most likely painful. As a result, the individual's daily physical activities would have been restricted to some extent. Reexamination of the age-at-death agrees with this individual being over 45 y old, relying on the modern human pattern of changes of the articular surfaces of the os coxae. The presence of degenerative pathological lesions and the advanced age-at-death of this individual make it the most ancient postcranial evidence of an aged individual in the human fossil record. Additional nonpathological SH lumbo-pelvic remains are consistent with previous hypotheses, suggesting a less-pronounced sagittal spinal curvature in Neandertals compared with Homo sapiens.

Uncovering the adult morphology of the forearm bones from the Sima de los Huesos Site in Atapuerca (Spain), with comments on biomechanical features.

The forearm skeleton is composed of two bones: the radius and the ulna. This is closely related to manipulative movements. The ulna is part of the elbow joint, whereas the radius and ulna together with the scaphoid and lunate bones, form the wrist joints. Thus, morphofunctional analysis of the adult Sima de los Huesos (SH) forearm bones, provides clues about manipulative activities in one Pleistocene population. From 1976 to the present, over 7000 human fossils have been recovered from the SH site. The radial sample comprised 98 labeled fragments, of which 49 belonged to adult individuals, representing at least 7 individuals. The ulnar sample included 31 labeled adult fossils representing at least nine individuals. In this study, we describe the SH radii and ulnae and analyze their functional implications for manipulative and forearm movements. We confirmed that the SH radii are long and curved, with variations in robusticity and radial tuberosity orientation. The SH ulnae are characterized by an anteriorly oriented trochlear notch, a massive olecranon process, an obliquely oriented radial notch, a blunt and short supinator crest, a gracile and curved diaphysis, and a round and anteriorly oriented pronator crests. In general, they exhibit Neanderthal morphology. The SH collection provides a unique opportunity to conduct morphological analyses of these bones in the Middle Pleistocene population.

Main anatomical characteristics of the hominin fossil humeri from the Sima de los Huesos Middle Pleistocene site, Sierra de Atapuerca, Burgos, Spain: An update.

Some of the Sima de los Huesos (SH) humeri have been previously studied and described elsewhere. Here we present an updated inventory and a review of the specimens recovered to the present day. The morphological key traits of the adult and subadult specimens are described, discussed, and illustrated. The SH humeri share with Neandertals many traits usually considered to be Neandertal specializations, thus, most of this morphological pattern is not exclusive to them. The variation found within fossil samples stresses the frequential nature of all these traits and in the specific case of the SH humeri, most of the traits considered as phylogenetically relevant are retained by their descendants, the Neandertals. Some traits are plesiomorphic for the entire genus Homo or are present in European hominins since the early Pleistocene. Finally, some other traits display high variability within the SH sample or different hominin samples and are of uncertain phylogenetic value. Altogether, this evidence is consistent with the hypothesis based on the overall cranial and postcranial morphology that the SH hominins are a sister group to the later Neandertals.

Exploring the morphology of adult tibia and fibula from Sima de los Huesos site in sierra de Atapuerca, Burgos, Spain.

The analysis of the locomotor anatomy of Late Pleistocene Homo has largely focused on changes in proximal femur and pelvic morphologies, with much attention centered on the emergence of modern humans. Although much of the focus has been on changes in the proximal femur, some research has also been conducted on tibiae and, to a lesser extent, fibulae. With this in mind, we present one of the largest samples of the same population of human tibiae and fibulae from the Middle Pleistocene to determine their main characteristic traits and establish similarities and differences, primarily with those of Neanderthals and modern humans, but also with other Middle Pleistocene specimens in the fossil record. Through this study, we established that the Middle Pleistocene population from the Sima de los Huesos (Atapuerca, Burgos, Spain) had lower leg long bones similar to those of Neanderthals, although there were some important differences, such as bone length, which this fossil individuals resembled those of modern humans and not to Neanderthals. This fact is related to the crural index and leg length, even though we do not have any true association between femora and tibiae yet, it has implications for establishing locomotor efficiency and climate adaptation.

Main morphological characteristics and sexual dimorphism of hominin adult femora from the Sima de los Huesos Middle Pleistocene site (Sierra de Atapuerca, Spain).

The excellent fossil record from Sima de los Huesos (SH) includes three well-known complete adult femora and several partial specimens that have not yet been published in detail. This fossil record provides an opportunity to analyze the morphology of European pre-Neandertal adult femur and its variation with different evolution patterns. Currently, there are a minimum of five adult individuals (males or females). In this study, we compiled previously published basic anatomical and biometric characteristics of SH adult femora, emphasizing the most relevant features compared to other recent and fossil hominins. The SH femora exhibited a primitive morphological pattern common to all non-Homo sapiens femora, as well as most of the Neandertal traits. Therefore, the complete Upper Pleistocene Neandertal pattern was well-established in Middle Pleistocene ancestors long before the proper Neandertals appeared. Additionally, we highlight that the SH and Neandertal femora share some morphological traits and proportions with modern humans that hold sexual significance in our species, regardless of size. Keeping this in mind, we discussed the sex determination of the complete SH specimens and re-evaluated sex allocation in two of them.

Updated study of adult and subadult pectoral girdle bones from Sima de los Huesos site (Sierra de Atapuerca, Burgos, Spain). Anatomical and age estimation keys.

Here we present an updated inventory and study of pectoral girdle remains recovered from the Sima de los Huesos (SH) site. Here, we describe the key morphological traits of adults and, for the first time, subadult specimens. Because morphological traits can change with age, we also discuss some shortcomings related to age estimation in postcranial fossil specimens. Adult clavicles from the SH are long with a low robusticity index and marked curvatures in the superior view. Among these traits, only extreme clavicular length seems to characterize subadult individuals. Neandertals share all these traits. In the case of the scapula, the SH specimens share a relatively long and narrow glenoid fossa with Neandertals. This trait is also present in subadult individuals. Additionally, most specimens from SH, adults, and subadults showed a dorsal axillary sulcus on the scapular lateral border, a trait also present in most adult and subadult Neandertals. These traits in adult and subadult specimens supports substantial genetic control for many of them in both human species.