Sima De Los Huesos

The Sima de los Huesos hominins are a 430,000 year old population of "pre-Neanderthals" from the archeological site of Atapuerca, Spain. They are in the "Neanderthal clade", but fall outside of ''Homo neanderthalensis''. When first published in 1993, these 29 individuals represented about 80% of the Middle Pleistocene human fossil record, and they preserve every bone in the human body. The unprecedented completeness of the remains sheds light on Neanderthal evolution, the classification of contemporary fossils, and the range of variation that could exist in a single Middle Pleistocene population. Exhumation of the Sima de los Huesos hominins began in the 1980s, under the direction of Emiliano Aguirre, and later Juan Luis Arsuaga, Eudald Carbonell, and José María Bermúdez de Castro.

As a pre-Neanderthal population, the Sima de los Huesos hominins display a mosaic of classic Neanderthal traits (apomorphies) as well as more archaic traits (plesiomorphies). Like in Neanderthals, the brow ridges are inflated, but the back of the skull is not as robust, and the skull has a "house-like" profile instead of the rounded "bomb-like" profile. Brain volume averages , on the lower end of the Neanderthal range of variation. The teeth are essentially Neanderthal-like, with shovel-shaped incisors and taurodontism, but they differ in tooth cusp morphology. The chest and waist are broad and robust like in Neanderthals, but the limbs are longer. They may have been overall large-bodied, with dimensions of about and for both males and females.

The Sima de los Huesos ("bone pit") is a chamber inside the Cueva Mayor – Cueva Silo cave complex at Atapuerca, and may have been a natural trap that creatures fell into — especially the cave bear ''Ursus deningeri''. The Sima de los Huesos hominins, on the other hand, may have been intentionally deposited into the pit by other humans, based on the quality of preservation, and the predominance of adolescents and young adults over children and elderly (catastrophic mortality profile), who were all buried at about the same time. One individual may have been murdered with a blunt tool. Some individuals with severe health issues survived for quite some time, evincing group care. Many individuals, especially adolescents, present several metabolic and malnutritional diseases altogether consistent with insufficient fat reserves during hibernation. Hibernation maybe lasted four months.

This population was producing Acheulean stone tools, as well as an industry seemingly transitioning into the typically-Neanderthal Mousterian culture. They used these tools in butchering, as well as in hide- and woodworking in combination with the mouth as a third hand. The Sima de los Huesos hominins were buried with a single, large Acheulean handaxe, possibly a grave good with symbolic significance. Symbolic thought could indicate the use of an early form of language. They may have been efficient hunters — possibly outcompeting local cave hyenas — pursuing deer, rhinoceros, horse, bison, and (more sporadically) cave lion in an open woodland environment. They probably also regularly ate roots, and habitually squatted. They probably were not using fire.

Research history

Discovery

In 1868, Spanish engineers P. Sampayo and M. Zuaznávar published a monograph documenting the many caves in the Sierra de Atapuerca, noting reports of human fossils in one (Cueva Ciega). In 1910, Spanish archeologists and Saturio González discovered a cave painting of a horse in Cueva Mayor, and the area quickly generated international interest. The eventually-abandoned construction of a railway (which was supplied by material mined out of what became known as the Trinchera del Ferrocarril) revealed that the Cueva Mayor was part of a larger cave complex — the Cueva Mayor – Cueva Silo complex. Its archeological significance was first understood in 1962 after exploration by the Edelweiss Speleological Group, who would identify several sites here strewn with Neolithic, Chalcolithic, and Bronze Age artifacts. While working on his doctoral thesis, Trinidad Torres unsuccessfully searched for bear fossils in the Trinchera del Ferrocarril, but was pointed by the Edelweiss Spelaeological Group to the unmapped Sima de los Huesos ("bone pit") in the Cueva Mayor – Cueva Silo complex. Sampayo and Zuaznávar had marked this as El Silo ("storage pit"), a chamber down a vertical shaft in the corner of the spacious Sala de los Cíclopes.

Torres sent four speleologists who identified a wealth of cave bear fossils (''Ursus deningeri''), as well as a nearly complete human jaw fossil. He notified his PhD advisor, Emiliano Aguirre, who organized further digs. The Sima de los Huesos was difficult to access, low in oxygen, and had been disturbed by many visitors over decades looking for bear fossil trophies — requiring much more excavation to remove the disturbed sediments ("revuelto"). In 1983, Aguirre found three fossil human teeth (as well as more bear fossils) in his brief visit to the Sima de los Huesos. Removal of sediment began the following year after installing lights and other necessary infrastructure. In 1987, Aguirre's team installed suspended scaffolding over the floor of the Sima de los Huesos to walk on. Large sediment blocks were transported up the vertical shaft (the only entrance), carried out through the mouth of Cueva Mayor with backpacks, driven out to the nearby River Arlanzón, dried, sieved, and later sorted. The "Atapuerca Team" under Aguirre had reconstructed three crania, one of which was nicknamed "Lazarus" — the first fossil from the site given a nickname.

Aguirre retired in 1990, and left excavation in the hands of his three team leads: Juan Luis Arsuaga, Eudald Carbonell, and José María Bermúdez de Castro. In 1992, a nearly complete skull (nicknamed "Agamemnon") was found; at the time only three other European skulls predating the Late Pleistocene had come close to such a level of preservation (Swanscombe, Petralona, and Steinheim). Soon after, another nearly complete skull was discovered, nicknamed "Miguelón" after Spanish cyclist Miguel Indurain. It is one of the best preserved skulls in the human fossil record. In 1994, a nearly complete pelvis ("Elvis") was discovered; at this time, the only equivalently preserved hominin pelvis predating the Late Pleistocene was the 3.2 million year old "Lucy".

Since then, over 7,000 human fossils and fragments have been recovered from the Sima de los Huesos, representing every bone in the skeleton. The material was preliminary thought to represent 32 individuals, but it more likely comprises 29. When first published in 1993, it was the most complete sample of the Middle Pleistocene human fossil record from a single site, representing 80% of the Middle Pleistocene human fossil record globally, and 85% of Middle Pleistocene postcranial (body) fossils. A similarly rich Middle Pleistocene human fossil assemblage would not be found until 2013, with the discovery of ''Homo naledi'' in South Africa. The Sima de los Huesos fossils elucidated the range of anatomical variation that could be present in any given population of Middle Pleistocene Europe — including across sex and age. Consequently, it clarified the relationships between Middle Pleistocene European fossils, as well as the evolution of Neanderthals. The great archeological significance of the Sima de los Huesos and other sites in the cave complex led to UNESCO declaring the archeological site of Atapuerca a World Heritage Site on 30 November 2000. To commemorate its cultural heritage, the city of Burgos about east opened the Museum of Human Evolution.

Age and stratigraphy

The Cueva Mayor – Cueva Silo complex is the main cave system of the Sierra de Atapuerca, extending over and three distinct levels — Sima de los Huesos at the lowest one. There are 4 entrances: Portalón (the entrance to Cueva Mayor) and Galería de las Estatuas in the first level, Sima del Elefante in the second, and Cueva del Silo in the third. Cueva del Silo is the nearest entrance to Sima de los Huesos, via the spacious Sala de los Cíclopes.

The Sima de los Huesos is underground, and from the entrance to Cueva Mayor. It runs at longest east-to-west, with a mostly horizontal segment (Sima Top), a 30° ramp (Sima Ramp) running down , and another horizontal segment (Sima de los Huesos proper). The cave infill is divided into 12 lithostratigraphic units (LU). The ramp has three test pits where fossils were collected: Alta (SRA), Media (SRM), and Baja (SRB). There are three chimneys: Chimney 1 between Alta and Sima Top, Chimney 2 between Media and Alta, and Chimney 3 above Sima de los Huesos proper. Chimney 2 is the only open one, leading into Sala de los Cíclopes to the west and a low inclined conduit to the east. It is the only entrance. Most of the human and carnivore fossils come from a section on the north side near the base of the ramp (on Sima de los Huesos proper) in LU-6. Additionally, over 100 human fossils were found along the ramp. A few human fossils were recovered from LU-7 where LU-6 had mostly or completely eroded away, which were probably reworked from LU-6.

LU-6 is a red clay layer of variable thickness, up to . It is composed of over 80% phyllosilicates, of which more than 60% is paramagnetic illite, permitting paleomagnetic dating to the Brunhes Chron; indicating that LU-6 is younger than 780,000 years. The fossils are randomly mixed into a bone breccia alongside limestone blocks, speleothem fragments (probably reworked from LU-2 and 4), marl clay chips (maybe from LU-1), and sometimes laminated pure mud (silt sized clay) rich in manganese dioxide. There are also ''in situ'' (not reworked) speleothems made of calcite rafts formed from undisturbed, seasonal pools of water; uranium–thorium dating of these rafts suggests a minimum age of 410,000–460,000 years (most likely about 430,000 years ago). Congruently, the overlying LU-7 is dated to 428,000 ± 27,000 to 441,000 ± 25,000; or 396,000 ± 35,000 to 429,000 ± 32,000 years ago; based on luminescence dating of respectively orthoclase and quartz. Luminescence dating of quartz grains from the underlying red clay suggests a maximum age of 448,000 ± 15,000 years ago.

The human material probably represents a single population. The limited carnivore damage suggests that the human fossils were largely inaccessible once buried. Only Chimneys 1 and 2 (via the incline conduit) may have been open at the time of deposition — all the way to the surface — and possibly acted as natural traps which creatures (especially the cave bear ''U. deningeri'') fell into. The humans may have been intentionally cast down. The corpses and bones probably slowly slid down the ramp and collected at the bottom.

Similar fossils have also been recovered from the GII and GIII layers of Trinchera Galería (respectively, a partial adult mandible with two molars, and an adult braincase fragment) about away from the Sima de los Huesos. This sequence extends continuously from 408,000–598,000 years ago; to 221,000–269,000 years ago. The roughly 300,000 year old Trinchera Dolina 10.1 layer in the Gran Dolina, about north of Galería, preserves a rich lithic assemblage. These sites were probably occupied by the same population as the Sima de los Huesos hominins.

Classification

In a 1993 preliminary report of the human fossil discoveries from Sima de los Huesos (at the time about 700 fossils representing the entire skeleton), Arsuaga and colleagues noted the many distinctly Neanderthal traits (apomorphies), and characterized the material as an early stage in Neanderthal evolution.

When the Sima de los Huesos fossils were discovered, Middle Pleistocene European and African fossils were usually classified as ''Homo heidelbergensis'', a wide-ranging species which was considered the last common ancestor of modern humans and Neanderthals. Arsuaga and colleagues instead believed Europe was more isolated from Africa, and placed the 1 million year old ''Homo antecessor'' (from the Gran Dolina) as the last common ancestor. They further believed that every Middle Pleistocene European fossil was part of a single population (''H. heidelbergensis'') ancestral to Neanderthals. In 2002, British physical anthropologist Chris Stringer instead suggested classifying the Sima de los Huesos hominins as archaic Neanderthals, but conceded they could be an extremely late ''H. heidelbergensis'' group. In 2011, Arsuaga and colleagues failed to identify Neanderthal apomorphies in the holotype specimen of ''H. heidelbergensis'' — the jawbone Mauer 1 — and questioned the applicability of ''heidelbergensis'' to more derived specimens (with Neanderthal apomorphies). In 2012, Stringer reaffirmed that the Sima de los Huesos hominins are much more derived than other Middle Pleistocene specimens (including Mauer 1), and should be moved from ''H. heidelbergensis'' to ''H. neanderthalensis''. In 2014, Arsuaga and colleagues agreed with Stringer — recognizing two distinct groups in Middle Pleistocene Europe — but were unsure whether species or subspecies distinction from ''H. neanderthalensis'' was more appropriate.

In 2014, mitochondrial DNA (mtDNA) was extracted from Femur XIII, which suggested that this individual shares a closer common ancestor with Central Asian Denisovans (the sister group of Neanderthals) than with Neanderthals. In 2016, nuclear DNA (nDNA) analysis instead concluded that the Sima de los Huesos hominins are more closely related to (but are not) Neanderthals. Because mtDNA is inherited from mother to child, the Sima de los Huesos hominins may carry the ancestral Neanderthal/Denisovan ("Neandersovan") mtDNA lineage, which was replaced in Neanderthals by interbreeding with African migrants sometime later.

Further discoveries of complete mandibles at the Sima de los Huesos indicate clear distinction from Mauer 1. While the Sima de los Huesos cranial and mandibular anatomy has developed most of the Neanderthal apomorphies (the earliest appearance for many of them in the fossil record), the rest of the skeleton retains many ancestral features (plesiomorphies), and nDNA indicates that they are a distinct group. They are, nonetheless, firmly nested in the "Neanderthal clade". Their anatomy also suggests that many Neanderthal apomorphies evolved by the mid-Middle Pleistocene, and the rest appeared late near the beginning of the Late Pleistocene, maybe associated with the full speciation of ''H. neanderthalensis''.

The Sima de los Huesos hominins can be grouped as "pre-Neanderthals", which can also include specimens from Montamaurin-La Niche, Pontnewydd, Steinheim, Swanscombe, and Aroeira. This group may ultimately descend from a Near Eastern source population which dispersed across Europe in the mid-Middle Pleistocene — maybe the same one represented at the contemporaneous Israeli Qesem cave, which is dentally similar to the Sima de los Huesos hominins. The timing might coincide with the end of a major glaciation event during Marine Isotope Stage 12 (the Elster/ Mindel/Anglian glaciation) roughly 450,000 years ago, during the warm interglacial period of Marine Isotope Stage 11. These "pre-Neanderthals" give way to "early Neanderthals" by the end of Marine Isotope Stage 7 (the Penultimate Glacial Period). "Early Neanderthals" are differentiated by a combination of both derived and "incipient" Neanderthal traits, and are succeeded by "late" or "classic Neanderthals" by the end of Marine Isotope Stage 5e (the Last Interglacial).

Skeleton

Skull

Cranial vault

The Sima de los Huesos material comprises 17 skulls. Like other Middle Pleistocene European specimens, the skull thickness of the parietal bone at the asterion (where it connects with the occipital and temporal bones) is normally midway what is usually seen between Neanderthals and Peking Man (''H. erectus pekinensis''). Cranium 4, though, falls on the upper end of the Peking Man variation of thickness in the angular torus (a raised bar of bone at the junction of the parietal and temporal bones) at .

Compared to Neanderthals, the occipital bone (back of the skull) is less curved, and lacks the characteristic occipital bun. Like in modern humans and Neanderthals, and unlike in ''H. erectus'', the opisthocranion (the farthest-back point on the skull) is above the superior nuchal line. The opisthocranion lies at the peak of a flat or slightly convex, semicircular area which extends down to the inion; the area is dotted with circular pits ("cratered") that became smaller and more dense with age. This area in Neanderthals is characteristically sunken (suprainiac fossa) and smaller; it is a variable trait among Middle Pleistocene specimens. Below this area is a weak occipital torus (a horizontal line of bone projecting off the occipital bone) — much weaker than exhibited in Neanderthals. The torus is most noticeable near the center of the occipital bone and terminates before reaching the asterion. A similar occipital morphology is exhibited in the Swanscombe Skull, but its torus extends farther like in Neanderthals.

When the skull is viewed from the back, the sidewalls run parallel to each other and form a shallow sagittal keel running along the midline of the skull ("house-like" or "en maison" contour) like other European Middle Pleistocene specimens. In contrast, the contour of ''H. erectus'' converges more strongly at the top ("tent-like"), and in Neanderthals it is rounded ("bomb-like" or "en bombe"). Like in Neanderthals but unlike in many Middle Pleistocene specimens, the supraorbital torus (the brow ridge) is double-arched instead of forming a single, straight bar. The arches are not divided, but some specimens have a depression on the glabella (between the brows). When viewed from the top down, the skull projects farthest around the glabella.

Brain

The average brain volume for the 15 Sima de los Huesos skulls for which the metric is calculable is , ranging from . The average is comparable to other Middle Pleistocene non-''erectus'' specimens which are known to range from , and on the lower end of the range of variation for Neanderthals which are known to range from .

Like other archaic humans, the parietal lobe was proportionally smaller than in modern humans. Compared to Neanderthals, the Sima de los Huesos brain was generally broader (especially towards the back, though this probably does not relate to function). The encephalic rostrum (the frontmost part of the corpus callosum) was more expanded than in ''H. erectus'', but thinner and narrower than Neanderthals. In Neanderthals and modern humans, typically the left hemisphere is bigger than the right, related to an expanded Broca's area associated with language acquisition; in the Sima de los Huesos hominins, brain asymmetry is variable. Like in Neanderthals, the temporal lobe is narrow, which is associated with visual and olfactory memory. The occipital lobe (the visual cortex) is more expanded than in modern humans, but much smaller than in Neanderthals.

Face

The mid-face (the nose and above) exhibits developed prognathism (it juts out), to a similar degree as other Middle Pleistocene specimens but not as much as Neanderthals. The face and nose are much wider than in Neanderthals and the cheeks are higher. Like in Neanderthals and most modern humans, but unlike ''H. erectus'', the bottom rim of the piriform aperture (nose hole) is raised. Like in Neanderthals (though to a lesser degree), the anterior nasal spine and inferior nasal concha at the base of the piriform aperature are fused, and the lateral crests are so well defined that they extend all the way to and connect with the nasal spine/concha. Unlike in Neanderthals, the floor of the nasal cavity is flat instead of sloping down.

The dental and jaw anatomy is generally Neanderthal-like, and similarly the regions of the temporal bone which are functionally relevant to chewing align closely with Neanderthals (the other regions are more basal). The tooth rows are square-shaped, like in Petralona 1, and in some Neanderthals. The mandible is mostly like that of Neanderthals, but has multiple mental foramina, a high mylohyoid line at the level of the third molar, and a more vertical and developed chin. The presumably female jaws are much smaller and have smoother muscle attachments, especially at the gonoid and coronoid process of the mandible. The degree of sexual dimorphism here is notably larger than in modern humans.

The upper teeth are essentially Neanderthal-like, with large and strongly shovel-shaped incisors and canines, as well as taurodontism in the molars. Unlike in Neanderthals where they are common, tubercules on the incisors, canines, and molars (the cusp of Carabelli) are an infrequent trait. The back teeth are notably smaller and less complex than in most other archaic humans, more similar to recent humans. The incisors and canines of the lower teeth exhibit somewhat weaker shoveling than in Neanderthals. The morphology of the lower premolars and molars are generally Neanderthal-like, though there is a greater range of variation in cusp size and shape.

Size

The Sima de los Huesos hominins, like other archaic populations, seem to have had much heavier skeletons than modern humans, which presumably supported greater muscle mass, and equated to an overall heavier build. The skeletal weight of the Sima de los Huesos hominins may have been roughly 36% greater than that of the average modern human.

Based on 19 complete male and 5 complete female long bones (sex assignment based on the size of the bone), average adult height was rather tall for archaic humans — respectively . Sexing the femora based on anatomical landmarks reassigns some of the assumed-male femora to female, with one potentially female femur (FXIII) belonging to someone possibly reaching . In general, large female body size may not have been uncommon in archaic humans.

The body mass of the complete male Pelvis 1 ("Elvis") may have belonged to someone in weight, potentially up to . "Elvis" has one of the highest weight estimates of an archaic human.

Based on the tarsus, average height was about for males and for females, with an average weight of . The highest weight estimate is , similar to "Elvis". Based on the metatarsals and phalanges, average size was and for males and females, respectively.

In general, Middle Pleistocene height estimates range from — though there are a few taller individuals — and Neanderthals were slightly shorter on average.

Postcranium

Before the discovery of the Sima de los Huesos hominins, the characterization of the Early and Middle Pleistocene human body plan was based almost exclusively on the Kenyan Turkana Boy. This specimen was originally reconstructed to resemble the narrower modern human body plan rather than the stockier Neanderthal body plan (which has since been called into question with more fossil discoveries), implying that the Neanderthal body plan was a unique adaptation — presumably as a response to cold climates. Every bone in the human skeleton is represented by the Sima de los Huesos material, and postcranial remains make up about half of the material.

Torso

The rib material is largely fragmented, with only a complete 1st, 11th, and 12th rib identified. Because the 1st rib is thicker dorsoventrally (front-to-back), and the pelvis is bigger anteroposteriorly (front-to-back) and mediolaterally (left-to-right) than in both modern humans and Neanderthals, the Sima de los Huesos hominins may have had an expanded thorax (chest) like in Neanderthals. The wide thorax and pelvis may be the ancestral condition for humans, with the narrow form of modern humans evolving more recently, but this is difficult to test given the paucity of postcranial remains predating the Late Pleistocene.

The pelvic cavity of "Elvis" (a male) is so wide that a modern human baby would be able to pass through it; and a female's would have been even wider. This could indicate the Sima de los Huesos hominins were born with a bigger head and brain volume. A broad pelvis would impede abduction at the hip joint, and was compensated by flaring iliac crests and a long femoral neck. Still, this would have made movement much more energetically expensive, especially over long distances, compared to modern humans.

Like in Neanderthals, the atlas (first neck vertebra) is wide dorsoventrally (probably related to the large foramen magnum, where the spine connects into the skull), and the axis is craniocadually (top to bottom) shortened. The atlanto-axial joint (between the atlas and axis, important in rotating the neck) is mediolaterally expanded. Like other archaic humans, the spinous process (jutting straight out of the vertebra) of the 6th and 7th neck vertebrae are long and horizontal — although it is shorter and more inclined than in Neanderthals. The shorter and more stabilized neck of Neanderthals and the Sima de los Huesos hominins could be related to balance with the broad chest and pelvis; the semicircular canals in the inner ear (which affect balance) are similar to those of Neanderthals, but the posterior canal is lower, and the anterior canal does not exhibit the same degree of torsion. The differences, if functional, could be related to the larger average body size of the Sima de los Huesos hominins.

Like in Neanderthals, the lumbar vertebrae (lower spine) exhibit less curvature ( hypolordosis, "flatback") than in modern humans. Like in modern humans and Turkana Boy (as well as the australopithecine ''Paranthropus robustus''), the transverse processes jut out of the vertebra dorsolaterally (from the sides angled back), whereas the dorsal (back) orientation is not seen in Neanderthals.

Limbs

Like in Neanderthals, there is a sulcus (groove) on the dorsal side of the axillary border of almost all of the shoulder blades (by the armpit), as opposed to the ventral sulcus of any other hominin specimen. This could have functional implications for the mobility and structure of the shoulder joint. The glenoid fossa (where the shoulder blade connects with the humerus) is taller and narrower compared to modern humans. Like in Neanderthals, the head of the humerus has an oval cross-section, the lesser tubercle is bigger, the deltoid tuberosity is narrower, the bone of the shaft is thicker, and the olecranon fossa (which connects with the ulna) is broader and deeper. The ulna and radius are usually also characteristically Neanderthal, lending greater mechanical advantage in rotating the forearm, but some can fall instead within the range of variation of modern humans — implying Neanderthals lost some variability here. The forearm is also longer than in Neanderthals. The hand is well-adapted for mobility and a precision grip, like in Neanderthals and modern humans.

Like other archaic humans, the femur has a flattened neck, the shaft is mediolaterally expanded near the top, the neck-to-shaft angle is low, the gluteal tuberosity is large, there is not a true pilaster (a vertical ridge unique to modern humans), and the bone is thicker. These differences may be related to supporting the heavier and more robust archaic skeleton, and compensating for the broad pelvis. Like in Neanderthals, the patella (knee bone) has deeper articular (jointing) surfaces, which could be related to stability. Like in Neanderthals, the articular surfaces of the tibia are flat, and the proximal epiphysis (at the knee-end) has a large retroversion angle (rotated backwards), which would have stabilized the knee joint during bouts of intense activity. About a quarter of the tibiae bear evidence of wearing near the ankle consistent with habitual squatting, and similarly the medial malleolus (the ankle bone that connects to the tibia) is hypertrophied (enlarged). The tibial pilaster is strong, which is only seen in the 400,000 year old English Boxgrove Man. Compared to Neanderthals, the tibiae are proportionally longer, more similar to modern humans. Longer legs would mean they were more energetically efficient while walking than Neanderthals, but the quadriceps muscle had less mechanical advantage. Like in Neanderthals, the tibial shaft is ellipsoid, as opposed to the triangular shaft of Boxgrove Man and Kabwe 1. The fibula indicates the gastrocnemius and soleus muscles were shorter than in modern humans, indicating higher energy costs while moving.

Like other archaic humans, the trochlea (in the ankle) is tall, broad, and rectangular (as opposed to the wedge-shaped one of modern humans), but the head is narrower than in Neanderthals and modern humans. The shape of the trochlea may have improved dorsiflexion and plantarflexion (up and down motion) in the ankle. Nonetheless, like in Neanderthals, the smaller malleolar fossa (which connects to the malleolus) on the fibula indicates a narrower range of dorsiflexion than in modern humans, though it does stabilize the ankle better. Like in Neanderthals, the heel bone is long, which may have improved shock absorption to compensate for the larger build. The Sima de los Huesos hominins were probably bigger than Neanderthals, and similarly the sustentaculum talus (which supports the spring ligament) projects even farther out than in Neanderthals. Like in Neanderthals, the phalanges as well as metatarsals 3–5 have a broad base, and the big toe is wider. The metatarsals and phalanges, in general, are much broader and more robust than in Neanderthals, which may be related to their bigger size. They probably walked and ran with the forefoot striking the ground first.

Pathology

Diseases

Cranium 5 presents severe dental decay, moderate gum disease, and alveolar osteitis on the left side. All of the teeth exhibit excessive wearing. There is extensive alveolar bone loss, causing overeruption of the teeth; at least a third of the root of every tooth is exposed. This individual seems to have been treating his gum disease with a toothpick, and similar toothpick grooves are found in some isolated teeth in the Sima de los Huesos. The lower left third molar (M₃) exhibits chipping. The upper left first premolar (P³) seems to have been badly chipped in life, exposing the pulp cavity. The wound seems to have suffered from chronic infection, leading to periapical cyst and fistula formation with remodeling of the surrounding bone. The lower left incisors also formed cysts, with pulp cavity exposure likely stemming from excessive loading and wearing in life; the upper incisors are similarly heavily ground down. The infection seems to have progressed to orbital cellulitis in the eye, and may have eventually progressed to sepsis, leading to death.

About 40% of the teeth exhibit enamel hypoplasia resulting from bouts of nutritional stress, peaking at about 3½ years of age. This could indicate the weaning age, which was probably around 4 years of age in Neanderthals, like recent hunter gatherers. Neanderthals suffered even higher rates and more intense bouts of hypoplasia, either because their subsistence strategies were less efficient, or because they lived in harsher environments.

"Elvis", based on joint degeneration, may have lived for more than 45 years. He similarly had age-related degeneration: lumbar kyphosis (excessive curving of the lumbar vertebrae in the lower back), L5–S1 spondylolisthesis (misalignment of the last lumbar vertebra with the first sacral vertebra), and Baastrup disease on L4 and 5 (enlargement of the spinous processes). These would have caused lower back pain, significantly limiting movement, and may be evidence of group care.

The adolescent Cranium 14 was diagnosed with lambdoid single suture craniosynostosis (immature closing of the left lambdoid suture, leading to skull deformities as development continued). This is a rare condition, occurring in less than 6 out of every 200,000 individuals in modern humans. The individual died around the age of 10, suggesting it was not abandoned due its deformity as has been done in historical times, and received the same quality of care as any other child.

Hibernation

The adolescents, especially, present pathologies consistent with chronic metabolic and malnutritional diseases, which could be consistent with insufficient fat reserves during hibernation. The adults do not seem to have suffered to the same degree. Hibernation can be induced in modern humans with injection of 5′-AMP (a secondary messenger), which in hibernating animals is normally produced by brown adipose tissue.

The Sima de los Huesos fossils bear several signs of chronic kidney disease–mineral and bone disorder (CKD–MBD), indicated by frequent osteitis fibrosa and renal osteodystrophy (ROD). They similarly present signs of vitamin D deficiency (which proceeds from CKD), and resultant hypocalcemia and secondary hyperparathyroidism (2HPT). These diseases are exhibited altogether in hibernating animals with insufficient fat stores. Fat deficiency leads to the arrestment of lipolysis, preventing the release of vitamin D stored in the fat cells. It also boosts cortisol levels to aid fat catabolism at the expense of serum calcium levels; hypercortisolism ultimately progresses to kidney disease. Fat deficiency is a major source of hibernation mortality.

The relevant pathologies are as follows:
*Regular bouts of extreme vitamin D deficiency cyclically caused lines of arrested growth in the bone, consistent with acquired rickets (rachitic osteoplaques). The pubescent Cranium 9 presents four such osteoplaques of rachitic hyperostosis — four short adolescent growth spurts separated by arrested growth (dormancy), a pattern characteristic of arousal from torpor. In other words, this individual may have roused from hibernation four times in a probably four-month hibernation period.
*"Elvis" presents several brown tumors (a type of osteitis fibrosa), part of the recovery process from severe CKD–MBD, rickets, and 2HPT.
*Some fossils show calcification of soft tissue, consistent with calcium pyrophosphate dihydrate crystal deposition disease. In bats, this is caused by increased production of adenosine triphosphate (ATP) during lipolysis of brown adipose tissue, to produce heat during bouts of arousal from hibernation.
*The entire population seems to have regularly suffered from subperiosteal new bone growth and consequent bone resorption in many places (especially the phalanges as well as the lamina dura in the teeth), resulting from severe rickets, 2HPT, and osteomalacia as a consequence of ROD during the healing process.
*Some ribs present the rachitic rosary (bead-like growths near the sternum) stemming from renal rickets and 2HPT.

Like the cave bears at the site, the Sima de los Huesos hominins may have developed hibernation to cope with the frigid and lean winters. Similarly, one adolescent cave bear specimen from the Sima de los Huesos presents subperiosteal new bone growth resulting from rickets. The age demographic of the Sima de los Huesos hominins is skewed towards adolescents, which is also observed in hibernation-related mortality events. Hibernation does not seem to have been practiced by Neanderthals, possibly because they were metabolically better at withstanding the cold, and were more efficient hunters capable of sustaining themselves year-round.

Violence

Crania 3, 5, 7, 9, 11, 13, 14, and 17 display several perimortem fractures (injured around the time of death). These fractures may have originated while falling down the shaft — not necessarily while they were alive, but at least near the time of death. Only 4% of the long bone material presents perimortem fracturing, and they lack any major injuries. American archeologist Erik Trinkaus noticed a similar pattern in Neanderthals, and suggested individuals who could not walk or keep up with a group while moving between cave sites were left behind. If true, then only individuals without major trauma to the limbs would be found at cave sites (survivor bias). It is unclear if this can be applied here.

Cranium 17 presents two nearly identical, connected, rectangular perimortem depression fractures on the left frontal squama (Trauma 1 below and Trauma 2 above). The injuries are angled in acutely at different trajectories, respectively 32.5°–44.8° and 49.2°. The injuries are consistent with powerful blunt force trauma, passing through the bone into the brain. The identical shape (even baring the same notch in the same position) suggests that they were caused by the same object, and their different trajectories suggests that they were caused by two separate actions; so it is improbable this individual got these fractures from simply falling into the Sima de los Huesos, or being struck by randomly falling limestone blocks. They may be the result of an intentional attack by another human with a tool in the right hand, resulting in her death.

Similarly, there is evidence that the Sima de los Huesos hominins were predominantly right-handed; and in forensic medicine, multiple blows to the face above the hat brim is normally interpreted as an assault ("hat brim rule"). This further means that the individual represented by Cranium 17 was already dead before dropping into the Sima de los Huesos, and — lacking any carnivore damage — was most likely interred by other humans. The perimortem fracturing on Cranium 5 on the frontal and left parietal, as well as Cranium 11 on the left parietal, may have also originated from interpersonal violence. No defensive injuries on the arms have been discovered.

Interpersonal violence in the fossil record is difficult to demonstrate. , the only other specimens which bear some strong evidence of this in the human fossil record is the Neanderthal Shanidar 3 and the modern human Sunghir 1.

Culture

Paleoenvironment

The Sima de los Huesos hominins were associated with an unusually diverse carnivore assemblage: the cave bear ''U. deningeri'' (this population seems to have been mostly herbivorous), wolf (possibly ''Canis mosbachensis''), the red fox, the cave lion ''Panthera fossilis'', the European jaguar, the cave lynx, the pine marten, the least weasel, the European polecat, and the European badger. This may indicate a high-productivity ecosystem. Rodents and other small mammals are far less common, and large herbivores are absent, consistent with the characterization of the site as a natural pitfall trap. The cave hyena, which is a common occurrence in similarly aged sites across Europe, is mysteriously absent; it is possible that the Sima de los Huesos hominins were outcompeting them in the region. At TD10.1, there is evidence of cave lion hunting and butchery; exploitation of carnivores is rare in the Middle Pleistocene, and this may have been a sporadic occurrence. ''U. deningeri'' is the most common animal at the site, but is not found anywhere else in the Sierra de Atapuerca. They may have been especially susceptible to falling into the Sima de los Huesos as they needed to seek out caves to hibernate in annually. Three human ribs exhibit peeling, and may have been fed on by a bear which fell in.

Several well-preserved bat fossils (mostly greater mouse-eared bat and a few Mehely's horseshoe bat) as well as significant guano accumulation were also found, probably representing overwintering roosts. Early Pleistocene deposits seem to indicate bats roosted in the area year-round, but only seasonally in the Middle Pleistocene when human activity increased. While the deteriorating climate of the time may have altered roosting behavior, their inability to recover during warmer periods (as other small mammals did) may indicate that they were disturbed by local human activity. The rodent fossils are also well-preserved and show no signs of digestion (not deposited by owl pellets), so they probably tunneled in through some small crevice.

The Gran Dolina TD10.1 and Galería GII and GIII sites had: the fallow deer ''Dama clactoniana'', the red deer, the roe deer '' Capreolus priscus'', the giant deer ''Praemegaceros solilhacus'', the narrow-nosed rhinoceros, the wild horse, the European wild ass, the wood bison '' Bison schoetensacki'', and the Bonal tahr. These herbivores could have been prey items. Like Neanderthals, the Sima de los Huesos hominins may have had a hyper-carnivorous diet comparable to contemporary lions. Galería seems to have also been a natural trap, and humans were possibly making sporadic, planned trips to the site as a "complementary settlement area" to harvest animals that fell in. TD10.1 was most likely occupied long-term, and the inhabitants seem to have been transporting only the most nutritional parts of a prey item back to the cave.

The Sima de los Huesos hominins most likely lived during one of the coldest glacial phases of the last million years, which caused an aridification trend in Iberia. Today, wintertime temperatures of the Sierra de Atapuerca can drop to , and it could have been even colder during glacial periods. The mammal assemblage indicates a savannah-like, open woodland environment. Both humans and lions seem to have been following the expanding open woodland corridors of Europe. The pollen record also indicates the spread of grass at this time. Aside from grasses, pine was predominant, followed by mesic plants such as oak, birch, and beech. Extensive vertical scratches on the teeth indicate that the Sima de los Huesos hominins were commonly chewing abrasive (dirty) foods, such as unwashed roots and stems. Females tend to have longer scratches in the lower teeth, suggesting their diet may have been different from males.

Technology

No stone tools were found in the Sima de los Huesos, as it was probably never inhabited. The Galería and Gran Dolina sites, on the other hand, preserve expansive lithic assemblages. Knapping techniques evolved significantly over time, but in general the Galería assemblage fits within the Acheulean industry, a Lower Paleolithic technology. TD10.1 could represent the transition to the Mousterian industry, a Middle Paleolithic technology associated with Neanderthals.

In Galería, there is little debitage (wastage), suggesting the tools were predominantly made off-site, with only quick, simple retouching happening onsite. This suggests that the site was used as a temporary base camp. In GIIa (the older part), the tool assemblage is mostly represented by simple lithic flakes, followed by retouched tools, and unmodified cobble. Retouched tools were usually made using chert and quartz, and large cutting tools (handaxes and cleavers) were predominantly made from quartzite. Unusually, cobble seems to have been used to shape the larger tools. In GIIb, larger tools (which require more planning) were produced more frequently from pre-prepared flakes instead of cobble, and quartzite is often replaced by sandstone, chert, and limestone. It is possible GIIb represents an entirely new group from GIIa, with different tool-making traditions. These trends continue into GIII, but the knappers stop shaping the base of the tool. In GIII, fewer and more efficient strikes were used, cleaving off bigger flakes from a core, but making the end product less standardized. The tools are also generally shorter and wider.

TD10.1 preserves over 20,000 lithics, one of the archeologically richest sites in the Sierra de Atapuerca. This likely represents long-term occupation sequences, in addition to some short-term ones. Similarly, there is a predominance of flakes and debitage over large cutting tools, as well as a complete chaîne opératoire (all debitage and products made during the tool-making process are present). TD10.1 is otherwise comparable to GIII. Tools were mainly made of chert, but sandstone and quartzite became more popular over time. Some chert seems to have been collected from a source away, an unexpectedly long distance to obtain resources for such an early group of humans. These tools were probably used extensively for butchering, as well as hide- and woodworking activity. Similarly, dental wearing suggests that every individual was commonly using the mouth as a third hand to bite onto probably animal skin or vegetable fibers with the front teeth, while cutting the material with a tool.

Knapping techniques are generally unstandardized, but the gradual shift in raw materials caused the longitudinal method (striking a lithic core parallel to its long axis, better suited for harder quartzite) to become less common, in favor of the orthogonal method (striking a core perpendicular to its long axis). In Galería, this gradually gets replaced by the centripetal method (striking starts at the edge of the core and works inward) in combination with the longitudinal method. In TD10.1, the centripetal and discoidal methods (associated with the Middle Paleolithic Levallois technique, exercising more control over the final shape) become more popular.

The Sima de los Huesos hominins were probably not using fire; instead physiologically withstanding the cold climate with their large body size, and presumably high activity levels and metabolic heat. High quality evidence of fire usage in Europe appears after an interglacial during Marine Isotope Stage 9 (roughly 340,000 years ago).

Burial

There are many peculiarities in the taphonomy of the Sima de los Huesos hominins which could suggest that they were intentionally buried by other humans, instead of falling down a natural pitfall as in the case of the many cave bears at the site.

About half of the Sima de los Huesos material is represented by adolescents/young adults between 15 and 18 years of age. Infants (below 2 years) are absent, and children below 10 are unusually rare given the high infant mortality rate of recent hunter-gatherer societies. The few individuals who seem to have surpassed 30 do not seem to have survived into their 40s based on the degree of tooth wearing. The overrepresentation of young adults in their prime (catastrophic mortality profile) instead of children and elderly (attritional mortality profile) suggests that the accumulation does not represent multiple generations which lived and died in the cave, but rather a single high-mortality event. A lack of stone tools also suggests this was not a living space. Because the entire skeleton (including fragile pieces) is extremely well represented by numerous different individuals all found in the same narrow layer of sediment, the bodies were most likely deposited in the Sima de los Huesos completely intact at around the same time. They also by-and-large lack carnivore damage. Because Cranium 17 presents two identical fatal injuries (therefore presumably caused by the same hard object), this individual was likely already killed — maybe by another human — before being deposited in the Sima de los Huesos.

Additionally, a single Acheulean handaxe (nicknamed "Excalibur") was deposited with the bodies, the only lithic artifact found at the site. It is made of high-quality veined quartzite, which was rarely used in the region, and was quite large at and . It lacks any indication of wearing or usage, unless it was scrubbed away by sand over time. In the context of intentional burial, Carbonell and colleagues suggested it was left as a grave good — an early example of complex symbolic thinking.

Language

It is possible that the Sima de los Huesos hominins were speaking with some early form of language, especially considering the evidence of intentional burial and symbolic thinking. The Sima de los Huesos hominins had a modern humanlike hyoid bone (which supports the tongue), but this trait can exist without language and humanlike speech capacity. Judging by dental striations, they seem to have been predominantly right-handed, and handedness is related to the lateralisation of brain function, typically associated with language processing in modern humans.

The middle ear bones are comparable to Neanderthals and modern humans, maybe suggesting they could distinguish the higher frequencies necessary to discern speech (2–4 kHz). Still, the functional anatomy of the ear suggests that the Sima de los Huesos hominins had different hearing capacities than Neanderthals and modern humans. Like chimpanzees, the ear canal is long, and the eardrum and oval window are small and at a low angle. Uniquely, the tympanic cavity (which contains the middle ear bones) and aditus are large. The cochlea (which affects hearing) is more constricted than in Neanderthals in the first turn (of about three turns), reminiscent of chimpanzees. Like in Neanderthals and modern humans, the third turn is short, but is more strongly curved.

See also

* Altamura Man
* Ceprano Man
* Jebel Irhoud

Notes

References

Bibliography

*{{cite journal, first1=J. L., last1=Arsuaga, first2=I., last2=Martı́nez, first3=A., last3=Gracia, first4=C., last4=Lorenzo, title=The Sima de los Huesos crania (Sierra de Atapuerca, Spain). A comparative study, journal=Journal of Human Evolution, year= 1997, issn=0047-2484, pages=219–281, volume=33, issue=2, doi=10.1006/jhev.1997.0133, bibcode=1997JHumE..33..219A , ref={{harvid, Arsuaga, Martı́nez, 1997

1976 archaeological discoveries
Fossils of Spain
Prehistoric sites in Spain
Archaeological sites in Castile and León