THE HOMINIDS FROM THE SIMA DE LOS HUESOS: 'HOMO HEIDELBERGENSIS'
Human evolution in the Middle Pleistocene
The evolutionary process during the Middle Pleistocene eventually culminated in the human forms known to characterize the Upper Pleistocene: the Neandertals and modern humans, 'Homo sapiens'. Some of the most burning questions in human evolutionary studies can be traced to this time period. Not long ago, a heated controversy surrounded the question of whether modern humans, Neandertals and 'Homo erectus' were different phases of a single evolutionary continium, or if, on the other hand, they represented different evolutionary lineages. At the basis of this controversy, the how, when and where of the origin of our own species were being debated.
The scarcity of the fossil record during this time period made it possible to defend diametrically opposed viewpoints with the same fossils. The main problem lay in the singular nature of most of the discoveries, which were also widely separated in time and space. Because of this, it wasn’t possible to be sure what part of the anatomical variation between fossils was due to biological variability, to processes of somatic growth and development in the case of immature individuals or was a reflection of sexual dimorphism. To solve these problems, a large sample of biologically contemporaneous fossils including both men and women of varying ages was necessary. The sample of human fossils from the Sima de los Huesos is the only case known from the Lower and Middle Pleistocene that meets these conditions.
History of the discoveries
As discussed in "The Sima de los Huesos site" section (http://www.atapuerca.tv/atapuerca/yacimiento_huesos), the first discoveries of human fossils came in 1976, during a short paleontological excavation campaign undertaken by members of the Grupo Espeleológico Edelweiss de Burgos, directed by a paleontologist who specialized in fossil bears, Trinidad Torres, when a human mandible was identified among hundreds of bear fossils. The association of the mandible with remains of the Middle Pleistocene bear species 'Ursus deningeri' led Torres to realize the importance of the discovery, and he showed the specimen to Emiliano Aguirre, who recognized the archaic morphology of the fossil as characteristic of European Middle Pleistocene humans. In the following days, a detailed analysis of the fossils recovered in the excavation revealed the existence of several new human remains: several teeth, fragments of other mandibles and a piece of long bone and cranial fragment. Aware of the importance of the discovery, Aguirre organized an interdisciplinary team with the aim of excavating and studying the series of Pleistocene sites in the Sierra de Atapuerca. Obviously, the site that stirred the most interest was the Sima de los Huesos, where the human fossils had appeared.
Nevertheless, the Sima combined several special characteristics and conditions that made its excavation very difficult. For decades, this site had been frequently visited by amateurs who dug around in the uppermost levels of the deposit in the search for bear fossils. These activities broke and mixed up many human and bear bones. Other factors which added to the difficulty of excavation were the great distance from the mouth of the Cueva Mayor, more than half a kilometer from the site, as well as the rarefied air deep inside the cave. For these reasons, systematic excavation of the site wasn’t begun until 1984, although the year before, a prospection at the site yielded a couple of human teeth.
In the course of eight field seasons, from 1984-1991, the work in the Sima de los Huesos consisted of removing, without the benefit of machinery of any kind, nearly seven tons of limestone blocks as well as several more of sediments, which were washed, screened and meticulously searched for new fragments of human fossils. The total number of human fossils discovered this way reached 389. To this total, we have to add 54 more fossils, equally fragmentary, which were recovered in a small section of the site where the undisturbed sediments were exposed during the first field season. Obviously, the excavation of the in situ levels was and is conducted with the greatest caution, scrupulously following the archaeological method.
During the 1991 field season, the last of the disturbed sediments were removed. Since then, excavation of the remaining in situ levels has yielded more than 3,500 human fossils. Among these, the three crania discovered in 1992 stand out: Cranium 4 (a calotte referred to as Agamemnon in honor of the King of the Achaeans, conquerors of the city of Troy), Cranium 5 (referred to as Miguelón, for the king of the Tour de France, the cyclist Miguel Indurain) and Cranium 6 (a fairly complete cranium corresponding to an adolescent individual). The discovery of a complete pelvis in 1994, Pelvis 1 (referred to as Elvis, in honor of the King of Rock n’ Roll), also stands out.
Even today, we still don’t know the limits of the fossil-bearing deposits. The evidence suggests, however, that at most only a third of the site has been excavated, which means there is every reason to believe that the discovery of new human fossils will continue for many years to come.
Morphological characteristics of the Sima de los Huesos human fossils
The sample from the Sima de los Huesos has made it possible to approach a number of aspects about this form of humanity and has led to a better understanding of human evolution during the lapse of time between 500,000-150,000 years ago. Among the more than 6,000 human fossils from the Sima de los Huesos, in addition to skulls and teeth, we also have bones of the leg, the arm, the hand…For some of the bones of the body, the fossils from this site are the only representatives that exist in the world from the time period prior to the Neandertals. From this treasure trove of information, the researcher team at the Sima de los Huesos has been able to fully characterize the anatomy of the entire skeleton of the human species that is represented in the Sima de los Huesos. This represents a milestone in human evolutionary studies, since there is no other fossil human species, not even the Neandertals, that is known as thoroughly.
To date, the collection of human fossils from the Sima de los Huesos includes fourteen skulls, in different states of preservation. Among them, the most complete are the three crania discovered in the 1992 field season: Cranium 4, 5 and 6. To measure the brain size of the two adult specimens from the Sima de los Huesos, we used three different methods. First, we directly measured the volume of millet seeds needed to fill their braincases. The values obtained were 1,390 cm3 for Cranium 4 and 1,125 cm3 in the case of Cranium 5. Second, we took computed axial tomography (CAT) scans, every millimeter, of crania 4 and 5. These CAT scans were then analyzed in the computer and provided values of 1,370 cm3 for Cranium 4 and 1,091 cm3 for Cranium 5. Finally, based on computer-generated three-dimensional reconstructions of the skull from the CAT scans, we constructed a highly precise plastic/resin model of Cranium 5. From this, we made a mold of the inside of the braincase whose volume was measured twice by water displacement, providing values of 1,080 cm3 and 1,090 cm3, respectively.
Based on these results, we can assign Cranium 5 a brain volume of around 1,100 cm3, a value which is among the smallest in the African and European Middle Pleistocene fossil record. Asian fossils attributed to 'Homo erectus' generally have smaller values, with the exception of the Ngandong sample, which could date to the Upper Pleistocene. At the same time Cranium 4 has a brain volume of around 1,390 cm3, which places it among the largest in the global fossil record for this time period. Cranium 6, somewhat less complete and belonging to an adolescent individual of some 14 years of age, would probably have an intermediate brain size. The value obtained from the volume of millet seed necessary to fill the braincase in this skull is 1,220 cm3.
From what we have just seen, it doesn’t seem to make much sense to use the brain size in isolated fossils as a taxonomic criterion, in other words, to identify different species, among African and European Middle Pleistocene fossils. We can, however, say that the range of brain sizes in the human population represented in the Sima de los Huesos is clearly larger than those of 'Homo erectus' and 'Homo ergaster'.
The bones of the skull, especially the walls of the braincase, are thick in the Sima de los Huesos crania. Sagittal prominences are always present but variably developed on the frontal and parietal bones, but not at bregma or along the coronal suture. Cranium 4 shows an angular torus in the rear of the parietal bone, while this structure is weaker in Cranium 5 and absent in the rest of the sample. These sagittal and angular thickenings of the bone are primitive characteristics not found in Neandertals. Among other European Middle Pleistocene fossils, an angular torus is found on Arago 47 (France), but is absent on the specimens from Petralona (Greece), Steinheim (Germany) and Swanscombe (England).
In the Sima de los Huesos sample, the maximum cranial breadth is located in a low position, at the level of the supramastoid crests, or just slightly above the ear canals. Above this level, the cranial walls, when viewed from behind, run vertically and are slightly convergent superiorly. This morphology is also found in other Middle Pleistocene European fossils from Petralona, Swanscombe, Reilingen (Germany) and Steinheim. This condition is evolutionarily intermediate between: 1) the primitive condition of a low pentagonal profile and 2) the rounded profile which characterizes the Neandertals or 3) the high pentagonal profile seen in modern populations.
When viewed from the side, it can be seen that the upper margin of the temporal squama is high and arched. This is a trait which is shared by 'Homo antecessor', African and European Middle Pleistocene fossils, the Neandertals and modern humans, and which distinguishes these populations from the 'Homo erectus' lineage.
Continuing in side view, the Sima de los Huesos crania show a more rounded posterior cranial profile than in the “classic” Neandertals. Neandertal skulls are typically elongated in the rear, with a flattened area in the region of lambda, the point where the two parietal bones join with the occipital bone. Below this, the occipital plane shows what is known as an “occipital bun”, a large protuberance produced by the projection of the occipital bone characteristic of the Neandertals. In crania 4 and 5 from Atapuerca, a certain convexity can be appreciated in the occipital plane, which, while not as marked as in the Neandertals, is more convex than in 'Homo erectus'.
In the occipital bones (in the rear of the skull) of the Sima hominids, the morphology of the occipital torus stands out. This structure is a raised bar of bone which is straight when viewed from any angle and is most strongly developed in the center of the occipital bone. In the Sima skulls, it doesn’t extend laterally almost to the temporal bone, or even further, as in 'Homo erectus'. Among Neandertals, the torus is also centrally developed, but is depressed in the middle portion and shows two lateral projections. Further, just above the torus the Neandertals present a small depression in the bone with an irregular surface, known as a “suprainiac fossa”. This is one of the most characteristic Neandertal features of the skeleton. In the Sima de los Huesos occipital bones, just above the torus is an oval-shaped region with a rough and porous surface which is sometimes flat but is never clearly depressed. This morphology is interpreted as an incipient stage in the evolution of the suprainiac fossa, which became more accentuated in the Neandertals.
On the skull base, it should be mentioned that crania 4, 5 and 6 from the Sima don’t show the elongated foramen magnum, the hole where the spinal chord leaves the skull, which apparently characterizes Neandertal infants and adults.
The supraorbital torus, or browridge, in the Sima sample is always double-arched, unlike the morphology seen in 'Homo erectus'. The supraorbital torus in this species is straight when viewed from any angle, clearly situated in front of and separated from the frontal squama (the forehead) and defining a more or less triangular-shaped surface between the trigone and the temporal lines. On the other hand, in the Sima frontal bones there are different degrees of fusion and continuity of the supraorbital torus at the midline of the browridge. Further, the torus also appears twisted in some specimens, so that the part closer to the midline of the skull faces forward and the lateral parts face more upwards. Thus, as a group, the Sima fossils are close to the Neandertal morphology, although some individuals also approximate the morphology seen in other Middle Pleistocene specimens, such as Arago 21, Bodo, Broken Hill and Petralona. Finally, as in the Neandertals, nasion is not depressed.
The facial skeleton of Cranium 5 is large in relation to the braincase, more so than is the case among the Neandertals, and this undoubtedly primitive characteristic is not as marked in Petralona. Cranium 5 also shows a stronger facial prognathism than seen in the Neandertals. It is interesting to note that in both of these characteristics Saccopastore 1 (Italy) is the Neandertal which is anatomically closest to the Atapuerca cranium.
At the same time, Cranium 5 shows a series of characteristics associated with what is known in the Neandertals as midfacial prognathism, or projection of the middle part of the face, the nasal region. For example, wide nasal bones oriented fairly horizontally, an anterior position of both the anatomical point subspinale (at the base of the nose) and the tooth row relative to the zygomatic bone and, in the mandibles, the presence of a retromolar space. In Neandertals, the infraorbital plate is convex or completely flat, with no canine fossa, and is oriented between the sagittal and coronal planes. The coronal orientation (toward the front) is the primitive condition and is also found in modern humans. The lower margin of the infraorbital plate (the zygomatico-alveolar crest) is straight and runs obliquely. In Cranium 5, the infraorbital surface is smoothly concave in horizontal section, and the lower border is curved, rather than straight.
The Neandertal morphological pattern, then, is not completely developed in Cranium 5. Although this specimen doesn’t have a canine fossa, this structure does exist in the more fragmentary fossil AT-404, also from the Sima. The Middle Pleistocene skull from Steinheim shows a markedly flexed maxilla, even though this structure could be somewhat exaggerated due to artificial deformation of the fossil after it was buried. At the same time, the Petralona skull is more Neandertal-like than Cranium 5, as is the deformed face of Arago 21. That is, there is variation in the European Middle Pleistocene sample, and even within the Sima de los Huesos, in the midfacial anatomy, with some specimens more derived (i.e. Neandertal-like) than others.
Another typical characteristic of the facial skeleton in Cranium 5 is the presence of a very wide opening for the nasal cavity, both in absolute and relative terms. Neandertals generally have wide nasal openings, although they aren’t the only ones, with the African Middle Pleistocene skull from Bodo having the widest of all. Finally, the morphology of the lower nasal margin is derived in Neandertals, and while Arago 21 also seems to show the Neandertal condition, the fossils from the Sima show the primitive condition.
As a whole, the temporal bones from the Sima de los Huesos lack the specializations which characterize the 'Homo erectus' evolutionary lineage, including the great thickness of the tympanic bone, the extreme reduction of the postglenoid process (which is highly developed in the Sima specimens) and the absence of fusion of the styloid process to the base of the skull (which appears fused in all the Sima specimens which preserve this region).
At the same time, the Sima temporal bones don’t show some of the derived characteristics of the Neandertal population. Thus, no specimen from the Sima shows an anterior mastoid tubercle in the antero-lateral region of the mastoid process. In Neandertals, the mastoid process, the inferior projection of bone just behind the ear canal, doesn’t project as much from the skull base. In the adult specimens from the Sima de los Huesos, the mastoid process is well-developed, both in size and projection, while in the immature individuals it is much less developed and doesn’t project beyond the occipitomastoid region. This pattern of development is the same as that found in modern human populations, while the “classic” Neandertals are characterized by adults with little mastoid process projection, which doesn’t normally surpass the adjacent occipitomastoid region. The mastoid morphology of the Neandertals, then, can be explained as the retention of a juvenile characteristic, similar to what was suggested previously for the facial anatomy of 'Homo antecessor'. The anterior wall of the glenoid cavity, the jaw joint just in front of the ear canal, in the temporal bones of the Sima de los Huesos is inclined forward, which is a derived characteristic of the Neandertals as well as other European Middle Pleistocene fossils, such as Steinheim, Petralona and Bilzingsleben.
The most conspicuous characteristic in the dental sample from the Sima de los Huesos is the ratio of the size between the anterior teeth (in which we include the incisors, the canine and the first premolar) and the posterior teeth (which includes the second premolar and all three molars), which shows an extreme value when compared to the variation seen among other hominids. While the anterior dentition in the Sima sample is comparable in size to other European Middle Pleistocene and Neandertal populations, the posterior dentition is markedly smaller, nearly identical in size to living populations. This dramatic reduction in the posterior segment of the tooth row in the Sima people can be interpreted as an evolutionary parallelism with modern humans, which does not necessarily imply an ancestor-descendant relationship, but rather a similar adaptation in two separate species. Further, this size reduction has several consequences for the dental morphology of the Sima population. The molars decrease in size from front to back in various individuals, with the first molar being largest. In addition, the hypocone and hypoconulid, cusps located toward the back of the chewing surface of the molar tooth crowns, are absent in a good part of the second and third upper and lower molars, respectively.
Together with this distinctive trait, most of the dental characteristics in the hominids from the Sima de los Huesos are derived. Some of them are shared with other European Middle Pleistocene hominids and the Neandertals, such as the expansion of the pulp chamber in the molar roots, known as taurodontism. Others, such as the absence of a cingulum (an extra development of enamel on the outer surfaces of the tooth crown) or the presence of only one root in the lower premolars, are shared with modern humans.
One of the best represented bones at the site is the mandible, and they are often very well preserved. Many of them have appeared with some of their teeth still included in the tooth sockets, while in others, it has been possible to associated isolated teeth found at the site. Within the sample from the Sima de los Huesos, very robust mandibles have been found together with others that are very small as well as some that are intermediate in size, making it difficult to determine whether they represent large females or small males. Like all other fossil human mandibles, with the exception of H. sapiens, the mandibles from the Sima de los Huesos lack a bony chin. In addition, the mental foramen is located below the first molar and many specimens show a retromolar space, like the Neandertals.
The postcranial skeleton
More than half of the Middle Pleistocene postcranial bones in the world derive from the Sima de los Huesos collection. The postcranial skeleton from the Sima presents a mixture of primitive and derived characteristics. One of the most evolutionarily important characters is the pubic length, which is long in Pelvis 1. Neandertals also have long pubic lengths, but with a much flatter and thinner cross-section. The pelves preserved in specimens of the genus Australopithecus also show long pubic lengths, which tells us that this is the primitive condition. It is present in all hominids except modern humans, the only ones who show a short pubic length with a thick cross-section.
In contrast, the vertebrae, together with the facial bones and phalanges, are among the most fragile bones in the body. Nevertheless, the extraordinary preservation of the fossils in the Sima de los Huesos has made it possible to recover 75 vertebral elements, with the cervical vertebrae being the most abundant to date. Comparison with our own species has revealed a strong resemblance in overall size of the vertebrae. However, in some metric and morphological features, the vertebrae from the Sima de los Huesos are more similar to Neandertal individuals than to modern human vertebrae. Among the associations of individual vertebrae, there is one that stands out from the rest. During the last 14 years, the excavation team has recovered, reconstructed and associated all seven cervical vertebrae that make up the complete neck of Miguelón, Cranium 5 from the site. Thanks to this effort, it was possible to exhibit this association to the public for the first time in December of 2005 at the exhibition “Atapuerca and Human Evolution” while it was at the Museo Arqueológico Nacional in Madrid.
Minimum Number of Individuals
In paleontological research, it is a common practice to estimate the minimum number of individuals (MNI) of a certain species which are represented in a fossil sample. If we want to know the MNI of a vertebrate species, we begin by counting the bone which appears most often in the assemblage. Since most bones come in pairs, we must also distinguish the bones from the left side from those from the right. Nevertheless, the enormous importance of the sample of fossil hominids from the Sima de los Huesos merits a more thorough investigation to try to establish the total number of individuals represented in the collection. How do we determine this number? Before answering this question, let’s learn a little more about the processes which occur between the time when an animal dies until its fossilized remains are discovered by an archaeologist or paleontologist, a science known as taphonomy.
The structure, size and shape of a bone are essential factors that influence which bones better resist these taphonomic processes. Once they’re buried in the sediments, the bones are subjected to diverse biological and geological processes which affect their preservation or degradation. These processes lead to certain bones, such as the mandible, the occipital bone or the femur being preserved more often than others, and hence they appear in a higher frequency in the archaeological record.
Another important factor in the durability of the organic remains is their hardness. The enamel and dentine in the teeth are the most resistant substances in the mammalian skeleton. 97% of enamel and 75% of dentine is comprised of inorganic material in the form of calcium phosphate crystals (apatite). It shouldn’t be surprising, then, that collections of fossilized mammals contain a large number of dental remains, whether isolated, or included in the mandible and maxilla. The durability of the teeth and the solid bony structure of the mandible is an advantageous combination, which explains the high frequency of these elements in the mammalian fossil record.
With this in mind, the fossils which preserve better are also the best to use when trying to establish the MNI. Thus, each mandible, with or without teeth in their sockets, represents one individual. Given that each tooth only fits correctly into its own tooth socket, we should try to fit the maximum number of teeth possible into the available tooth sockets in the mandibles and maxillae. Many of the remaining loose teeth could belong to other individuals which we will try to identify. Each human being has their own personal dental characteristics. The size, shape, certain marks produced during the formation of the tooth (hypoplasias) and even the type and degree of tooth wear can be used to identify an individual.
Following these criteria we can conclude that the sample of human fossils recovered to date in the Sima de los Huesos corresponds to at least 28 individuals. This “family” is made up of one child, 13 adolescents between 10 years and 16/17 years of age, 7 adults between 17/18 years and 24/25 years of age and 7 adults older than 25/26 years. Of this last category, only three had survived beyond 35 years, but couldn’t have been older than 40/45 years of age at the time of their death. Pelvis 1 could represent one of these oldest individuals. The surface of the pubic symphysis, at the front of the pelvis, and the articular facets, where the bones meet, between the sacrum and the coxal bones indicate an age at death of older than 45 years. Another individual from the Sima, of which the pubis is preserved, could have also been older than 45 years.
The Sima de los Huesos humans: What were they like?
Studies of the postcranial skeleton, dentition, mandibles and crania suggest that both sexes are equally represented in the Sima de los Huesos sample. This is fortunate because it has allowed us to tackle the problem of sexual dimorphism, the size differences between males and females, in a Middle Pleistocene human population. This is a crucial question in human evolutionary studies since the degree of sexual dimorphism shows a correlation with certain social behaviors and organization among living primates.
In hominids, sexual dimorphism is mainly expressed in terms of body weight, with males being heavier than females. In the earliest hominids, these size differences were as marked as in the case of gorillas, where males weigh almost twice as much as females. In our own species, males and females are much more similar in size, with males being on average 10% heavier than females. However, it wasn’t known how sexual dimorphism had decreased during the course of human evolution, and various authors maintained opposing opinions.
The extraordinary sample of human fossils from the Sima de los Huesos, which includes numerous bones highly correlated with body weight (such as femora, foot bones, or the pelvis) has allowed us to perform a complex statistical analysis whose results are clear and somewhat surprising: the degree of sexual dimorphism in the population represented by the Sima de los Huesos was similar to that seen among ourselves.
Given that the size differences between the sexes was the same as in living humans, once you know the height and body size of one of the sexes you also know the characteristics of the other. For this purpose, the study of Pelvis 1 proved to be instrumental. In the first place, it was possible to determine that this individual was male, due to various anatomical details of the pelvis, such as the triangular shape of the upper pubic ramus, the narrow sciatic notch and the forward position of the joint between the coxal bone and the sacrum.
At the same time, based on several femur fragments which belong to the same individual as Pelvis 1, we have estimated the stature at around 175 cm (about 6 feet tall). This value is similar to the average height of male individuals in a living population and slightly taller than the average stature of the Neandertals.
In addition, the width of the pelvis is highly correlated with the width of the trunk of the body and the thorax, and this has allowed us to estimate the body weight of this individual as around 95 kg (about 210 pounds). Nevertheless, it is probable that this individual weighed more than 100 kg (220 pounds), since the formulas used for calculating the body weight were based on modern humans, who have a lighter body build. Nor does this take into account the fact that the bones themselves were heavier in these Middle Pleistocene hominids, with thicker cortical bone in the walls. Thus, both sexes of the Middle Pleistocene people of the Sima de los Huesos show very robust, heavily-built bodies.
Knowing the body weight of the Sima hominids is critical to addressing another important topic in human evolutionary studies: the degree of encephalization, or the relationship between brain size and body weight. As we saw earlier, we have very precise measurements of the brain size in two individuals from the Sima sample (Cranium 4 and Cranium 5), from which it is easy to estimate their respective brain weights. Although the average brain size in the Sima population is only slightly smaller than that of modern humans, their larger body size means that their degree of encephalization was clearly lower than ourselves. Even more interesting is the fact that the degree of encephalization in these Middle Pleistocene hominids was also clearly lower than that of their descendants, the Neandertals. Many authors had not accepted this idea, until the evidence from the Sima de los Huesos demonstrated it to be true.
Another important topic that can be analyzed in the pelvis is the mechanics of the birth process. Although Pelvis 1 belonged to a male individual, fragments of female pelves have also been found in the Sima. Comparing them has shown that the differences in shape between male and female pelves in the Sima de los Huesos are similar to the differences found in living populations, which allows us to reconstruct the shape a Middle Pleistocene female pelvis would have had. Women today have a larger pelvic canal, or birth canal, than men, and it would be almost impossible for a male individual to give birth successfully. Nevertheless, the pelvic canal of the Sima de los Huesos individual is so large that the head of a modern human infant could easily pass through it. Keeping in mind the great width of Pelvis 1, it is not difficult to conclude that Middle Pleistocene women would have had a larger pelvic canal than modern women. If we add to this the fact that newborns would have had a smaller head than modern infants, we can conclude that giving birth would have been more comfortable and less difficult than in our own species. Nevertheless, the physiology and mechanics of the birth process in the Middle Pleistocene would have been very similar. Since the spiral shape of the pelvic canal and the position of the vagina are the same as in living humans, the head of the fetus would also perform a double internal rotation (as in our own species) and would leave the womb facing upwards, rather than facing backwards as in other primates.
Health and Disease
Different pathologies have been described in the Sima de los Huesos sample. Among them, the high prevalence of degenerative temporomandibular arthropathy is notable, and affects both jaw joints on either side of the skull in almost every individual. Further, a severe bilateral hyperostosis of the external auditory canal (the ear canal) in Cranium 4 notably reduced the auditory capacities in this individual, perhaps even causing deafness. Cranium 5 suffered from a severe maxillary infection, brought on by a tooth fracture during the lifetime of this individual. The gravity of this infection is such that we cannot discard the possibility that it caused a septicemia which brought about the death of this individual. Another interesting pathology is also prevalent in a number of crania. Crania 4, 5 and 6 show scars on the cranial vault produced by light head injuries, and on Cranium 5 there are quite a few. The lateral part of the left browridge in the immature individual AT-624 suffered a severe blow which affected not only the outside table of the bone, but penetrated into the diploe of the cranial vault. However, there are signs of bone regeneration in this area, which suggests that the child didn’t die from this blow. Nevertheless, the inflammation would probably have caused vision problems in the affected eye. Finally, the mandible AT-772 + AT-792 lost both of the central incisors and the right lateral incisor from a frontal blow.
One of the most interesting indicators of health and general quality of life in previous populations are what is known as enamel hypoplasias. This is an anomaly or deficiency in the enamel mineralization process, or amelogenesis, which manifests itself as a depressed zone in the enamel in the tooth crowns, generally visible to the naked eye.
Enamel hypoplasia is considered evidence of a non-specific stress which occurred during development, and is associated with serious cases of malnutrition, certain illnesses, infections and trauma. In general, a higher prevalence of cases of hypoplasia in the population indicates a lower quality of life, in which a monotonous diet low in calories, poor in animal proteins and lacking certain vitamins and minerals can play an important part. The width and depth of the areas affected by enamel hypoplasia can tell us about the intensity of the stress suffered by a child during their growth and development. Since the onset and finish of crown formation is known for each tooth, as well as the length of the entire process, we can determine with relative ease the approximate moment when each episode of stress occurred according to the position of the hypoplasia on the tooth crown.
The analysis of 22 lower canines (21 permanent teeth and one deciduous tooth) recovered in the Sima de los Huesos can inform us about the prevalence of enamel hypoplasias in the population among children until roughly 5 ½ years of age, when the tooth crown is fully formed. These teeth belong to a total of 17 different individuals, of which only five show hypoplasias of a certain severity, indicating that somewhat less than 30% of the children in this population suffered from episodes of physical stress. This is less than the percentage (46.5%) observed in a large Neandertal sample and much less than certain populations of 'Homo sapiens' from different epochs, including some from the past century living in semi-industrialized societies.
It is interesting to point out that the majority of stress episodes detected in the Sima de los Huesos occurred during a very concrete period in infancy. In effect, the majority of the hypoplastic lines, grooves and bands occurred between 3-4 ½ years of age. The subject of the timing of maximum frequencies of hypoplastic defects has been observed in all the populations studied, although the moment of initial appearance is variable. Thus, the peak of maximum frequency in Neandertals coincides with that of the Sima (3 ½ years), while in modern historic populations, this peak usually appears earlier, between 1-3 years of age. It has been suggested that this peak of maximum frequency coincides with the weaning period in infants, that is, the period when a gradual reduction is taking place in the amount of maternal milk consumed and new foods are being added to the diet.
Another interesting health aspect of the Sima population is their apparent concern for dental hygiene. The necks of numerous premolars and molars in the collection show certain grooves produced by the use of “toothpicks” to clean these interdental spaces, and this practice could have had a therapeutic effect as well. These toothpick grooves are only present in those individuals with a certain degree of “exposure” of the tooth roots. That is, in individuals who suffered a loss of alveolar bone surrounding the tooth sockets, whether as part of the normal ageing process or due to periodontal disease, and which led to a certain opening of the interdental spaces. Small particles of food solids easily lodge in these spaces producing a more or less painful nuisance. If the food consumed also contained a certain amount of hard and abrasive particles, something that must have been common in Pleistocene hominid populations, this could produce abrasions that would facilitate the formation of such toothpick grooves. This practice of preventive hygiene among the Sima hominids is among the most ancient known.
According to all the available evidence, then, we can state that the population represented by the hominid sample from the Sima de los Huesos had an acceptable diet and quality of life, even when compared with certain recent human populations whose economy was based on agriculture and possessed a certain level of industrialization.
The place of the Atapuerca fossils within the human evolutionary tree
Some researchers have suggested that two main branches can be distinguished in the human evolutionary tree during the Lower and Middle Pleistocene, both of which evolved from 'Homo ergaster', who would represent their last common ancestor. On the one hand is the exclusively Asian branch of 'Homo erectus'. The other evolved independently from 'Homo erectus', is more complex, and includes the African and European Middle Pleistocene fossils which eventually gave rise to the Neandertals and ourselves, 'Homo sapiens'. In this scenario, the evolutionary lines of the Neandertals (in Europe) and modern humans (in Africa) would have diverged less than 500,000 years ago. Middle Pleistocene human fossils from Africa and Europe were grouped together in the species 'Homo heidelbergensis', who was said to be the last common ancestor of the Neandertals and modern humans.
Our analysis of the Sima de los Huesos human fossils has led us to conclude: 1) that all the European Middle Pleistocene fossils (including Mauer, Steinheim, Petralona, Arago, Swanscombe and the Sima de los Huesos, among others) correspond to the same evolutionary stock and 2) that derived traits shared with Neandertals are only found in these European Middle Pleistocene fossils. In other words, the Middle Pleistocene European hominid population, and only this population, were the ancestors of the Neandertals, but not of modern humans.
Based on these conclusions, two possibilities exist. If 'Homo heidelbergensis' is the common ancestor of the Neandertals and modern humans, then we should exclude the European Middle Pleistocene fossils from this species, since they are only the ancestors of the Neandertals. This isn’t possible, because 'Homo heidelbergensis' was defined on a European fossil, the Mauer mandible, which gave the species its name. Thus, any definition of which specimens comprise this species must necessarily include the Mauer mandible, a European Middle Pleistocene fossil. The second option is to consider Homo heidelbergensis as a “chronospecies” within the evolutionary line 'Homo heidelbergensis'/'Homo neanderthalensis' (or even a subspecies: 'Homo neanderthalensis heidelbergensis'). This hypothesis acknowledges an ancestor-descendant relationship between the European Middle Pleistocene fossils (such as from the Sima de los Huesos) and the later Neandertals, and recognizes that the line separating one from the other is difficult to draw. Thus, as a chronospecies, 'Homo heidelbergensis' is defined temporally as one part of a continuous European evolutionary lineage. As a consequence of this, we must look for an alternative candidate for the last common ancestor of this lineage and that of modern humans.
'Homo antecessor' could very well be this candidate. Since we’ve already detailed the anatomical evidence which lead us to propose an evolutionary relationship between this species and 'Homo sapiens', we must now address its possible relationship with the Neandertals, through intermediate populations like that of the Sima de los Huesos. 'Homo antecessor', 'Homo sapiens' and 'Homo neanderthalensis' share several evolutionarily derived cranial characteristics. The high, arched upper margin of the temporal squama, the anterior placement and vertical orientation of the maxillary incisive canal and the prominence of the nose are clearly similar in all three species. Together, these three anatomical characteristics form a pattern which is both common to all three species and exclusive to them, and forms a solid basis to propose that Homo antecessor was the common ancestor species for both the Neandertals and 'Homo sapiens'. We can also add here the fact, discussed previously, that certain specimens in the sample from the Sima de los Huesos (e.g. AT-404) and among the European Middle Pleistocene fossils (e.g. Steinheim) show a facial morphology which could be interpreted as intermediate between 'Homo antecessor 'and the Neandertals.
Our hypothesis of evolutionary relationships, then, argues that the Neandertal and modern human evolutionary lines were already separated in the Middle Pleistocene, a view which contrasts with that supported by other authors mentioned at the beginning of this discussion. Consequently, we propose that the European and African fossils from this time period should be named separately, with 'Homo heidelbergensis' reserved for the European specimens and 'Homo rhodesiensis' for the African fossils. We should emphasize that this species difference is based only on evolutionary relationships and does not necessarily imply that representatives of both lineages, who are after all still very similar, were different biological species. Thus, it is still possible that members of each lineage could have occasionally produced offspring and exchanged genes. Our hypothesis of evolutionary relationships, nevertheless, assigns 'Homo antecessor' the role of last common ancestor of both the Neandertal ('Homo neanderthalensis') and modern human ('Homo sapiens') lineages.
This scenario has been strengthened in recent years by two independent lines of evidence. Research into the mitochondrial DNA (mtDNA) extracted from the original Neandertal fossil, recovered from Feldhofer Cave in the Neander Valley in Germany, has produced some very interesting data on the timing of the separation of these two lineages. When the mtDNA sequence of the Neandertal specimen is compared with numerous sequences from diverse living populations of humans, the genetic differences between the Neandertal specimen and living populations is appreciably greater than the differences observed between the living populations themselves. By estimating the amount of time necessary to produce such a difference, it appears that the Neandertal and modern human lineages must have parted ways some 465,000 years ago, with a more conservative estimate being between 317,000-741,000 years ago. These dates are older than almost all of the human fossils which comprise the European and African Middle Pleistocene record, which, by being younger than the divergence date, means they would already have clearly pertained to one lineage or the other.
At the same time, in 1994, a skull was found at the site of Ceprano, in the region of Campogrande, not far from Rome, which is dated to between 800,000-900,000 years ago on the basis of comparisons of the site with the known stratigraphic sequence in the surrounding region. This cranium belonged to a very robust adult individual with a brain size greater than 1,100 cm3. The analysis of this fossil has lead its describers to conclusions which are practically identical to our own, and to contemplate its inclusion in Homo antecessor as very plausible.
Development and Age-at-death
Another basic question when dealing with fossilized remains is whether the specimen being considered was an adult or immature individual at the time of their death. The growth and development of the skeleton in a child can be followed with radiographic techniques (X-rays) from birth until adulthood is reached. In very general terms, a given age will correspond to a certain size and stage of development in the bones and teeth, within the normal ranges of variation which characterize any biological population.
The teeth can provide very useful information to address this question since they undergo a process of growth and development which is coordinated to some degree with that of the rest of the skeleton. Not only do we lose our “milk” teeth when they are replaced by the permanent dentition, but the stages of formation and eruption of each tooth correspond to a precise moment in the growth and development of a child, and can be easily studied in radiographs.
The sample of fossil hominids from the Sima de los Huesos includes dental remains of several children and adolescents. All we have to do is compare the formation and eruption stages of these teeth with the numerous studies carried out on modern populations to arrive at an age at death for these individuals.
To estimate the age at death of adult individuals (whose teeth are already fully formed) in previous populations, we must rely on the degree of tooth wear, although the results are much less precise than those obtained for the immature individuals. Once a tooth becomes functional, after it has fully erupted, the occlusal (chewing) surface immediately begins to wear down through use, as do the anterior and posterior surfaces which are in contact between adjacent teeth. This wear process proceeds faster or slower depending on the type of diet and the possible presence of abrasive particles in the food, which intensively polish the enamel and dentine in the teeth. Human populations from the Pliocene and Pleistocene, and even those from the Holocene, suffered a considerable degree of tooth wear, to the point where even in very young individuals the molar crowns could be worn down to the root, exposing the pulp cavity. Today, cooked foods and a rigorous hygiene have considerably reduced the speed and rate of tooth wear, which has been reduced to friction between the teeth during chewing.
One additional problem is that the speed of wear in the teeth varies from one population to another depending on the diet. To address this problem, the researcher A. Miles has proposed that we estimate the rate of tooth wear in immature individuals, whose age at death we know based on the formation and eruption stages of their teeth. Once we have established the rate of wear in immature individuals, we can then use this information to estimate the ages in adult individuals. Using this process, we have been able to estimate the age at death of the adults from the Sima de los Huesos with a reasonable level of precision, although still accepting a margin of error of plus or minus five years.
According to these data, the fossil humans from the Sima de los Huesos represent 28 individuals who died between 5 and 35 years of age.
Origin of the accumulation
One difficult question to answer is the origin of this accumulation of human fossils in the Sima de los Huesos. Not a single herbivore bone has been found at the site, and although the human remains present an occasional tooth mark (which we interpret as the result of bears which, as we will see shortly, fell down into the Sima and were alive for a brief period at the site) there are no signs they were eaten by predators, which rules out a carnivore den. At the same time, there are hardly any cubs among the carnivore species found in the Sima, only eight bear cubs among more than 167 adult bears. The 26 foxes are also all adults, as is the case with the remaining species, with the exception of an immature lion that could have been around 10 months old. So it’s difficult to interpret the site as a birthing place for these animals, since the proportion of very young individuals would have to be much higher.
In our opinion, the accumulation of bear remains is due to the Sima acting as a natural trap for these animals during periods of hibernation. This is a relatively common phenomenon and accumulations of living brown bears ('Ursus arctos') as well as cave bears ('Ursus spelaeus') are known to have occurred at the bottom of pits. The presence of other carnivores can be similarly explained. It isn’t difficult to imagine that the stench of carrion from fallen bears could have attracted other carnivores, some of which accidentally fell into this natural trap.
Nevertheless, the explanation for the accumulation of human remains at the site is more problematic. In the first place, the analysis of skeletal part representation carried out on the collection of human fossils indicates that all parts of the skeleton are represented, which demonstrates that the original accumulation consisted of cadavers and not isolated bones. At the same time, the complete absence of prey species and stone tools (see below) indicates that this was not a human occupation site.
In our opinion, the evidence clearly points to an anthropic (human) origin for the accumulation of the human remains, having been deposited in the Sima by other humans. In this context, the discovery of a stone tool during the 1998 field season, the only discovery of its kind during 19 field seasons and among literally thousands of human and animal fossils, is particularly relevant. The piece in question is a handaxe, the most emblematic stone tool of the Acheulean industry. This handaxe, referred to as Excalibur in honor of the magical sword of King Arthur, is one of only a few found to date in any of the sites in the Sierra de Atapuerca, in which this type of artifact is very rare. Further, the singular nature of this discovery is underscored by the fact that it was made of a type of stone which is also rare in the other Atapuerca sites: red quartzite.
If future discoveries and research strengthen our hypothesis on the intentional origin for the accumulation of the human cadavers in the Sima de los Huesos, we would be witnessing one of the most important discoveries made in Atapuerca: the oldest evidence of funerary practice, and hence symbolic thought, in the history of humankind.