Sunday, June 22, 2014

Neandertal roots: Cranial and chronological evidence from Sima de los Huesos

Vol. 344 no. 6190 pp. 1358-1363
DOI: 10.1126/science.1253958


[Blog note:  This paper, elucidating the anatomical features of the Sima de los Huesos skulls, has been widely covered in the press in the last few days.  For instance, in the GuardianNeanderthal faces emerge from the gloom of a Spanish cave.  Rather than commenting, I thought I would make it easier for the general public to access essential sections of the paper. (I have not included the intermediate sections on dating of SH (Sima de los Huesos), cranial capacities and encephalization quotient, cranial vault comparisons, facial skeleton, basicranium, or mandibles and dentition.)  For interested readers who are non expert in the area of cranial morphology, supplementary section S2 provides descriptive statistics on the parameters discussed.  Additionally, several youtube videos are helpful: cranial anatomy and cranial landmark definitions.  Some of the skull features discussed are ones that most people are aware of on their own head:  the occipital structure on the back of the head, the bumps on the side of the head above the ear, and various structures on the front of the face such as the brow and jaw.  The intermediate sections of the paper discuss how these vary in the SH specimens and other hominins and for this reason, a careful reading of the full paper is instructive toward understanding the points made in the discussion section.]


Seventeen Middle Pleistocene crania from the Sima de los Huesos site (Atapuerca, Spain) are analyzed, including seven new specimens. This sample makes it possible to thoroughly characterize a Middle Pleistocene hominin paleodeme and to address hypotheses about the origin and evolution of the Neandertals. Using a variety of techniques, the hominin-bearing layer could be reassigned to a period around 430,000 years ago. The sample shows a consistent morphological pattern with derived Neandertal features present in the face and anterior vault, many of which are related to the masticatory apparatus. This suggests that facial modification was the first step in the evolution of the Neandertal lineage, pointing to a mosaic pattern of evolution, with different anatomical and functional modules evolving at different rates.


The course of human evolution in the Middle Pleistocene is controversial (1, 2, 3, 4). Most of the debate has focused on taxonomic and phylogenetic questions, particularly surrounding the origin of Neandertals and modern humans (5, 6, 7, 8, 9). The European Middle Pleistocene fossil record is important for the timing and pattern of emergence of the Neandertals, but it is composed mainly of isolated and geographically dispersed remains of diverse chronologies. This complicates the evaluation of competing evolutionary scenarios. One of these scenarios, known as the “accretion model,” rests on two hypotheses: one regarding the timing of the origin of the Neandertal lineage and the other regarding the pattern of morphological change (1, 5, 10). Under this model, the Neandertals would have deep roots in the Middle Pleistocene, branching off as early as Marine Isotope Stage 11 [around 400,000 years ago (400 ka)] (5, 11), or even earlier. In addition, the model suggests that the full suite of derived Neandertal features (anatomical and functional modules) did not emerge as a single package, but that different features appeared separately and at different times. In particular, Neandertal facial morphology evolved first, followed by changes in the neurocranium.
Here we analyze a collection of 17 well-dated skulls, including several previously unpublished specimens [Fig. 1, supplementary text S1 (12), and table S1], that can be used to test the two pillars of the accretion model. This sample comes from the Sima de los Huesos (SH) Middle Pleistocene site in the Sierra de Atapuerca (Spain) and derives from a single paleo-deme (p-deme). Because the accretion model is based mainly on nonmetric traits (5), our analysis emphasizes the pattern of expression of morphological features in the SH hominins, although the descriptive statistics for the principal craniometrical variables in the SH sample are also provided (table S2).

    Fig. 1    Cranium 9 (top left), Cranium 15 (top right), and
    Cranium 17 (bottom) from SH.  (Scale bar: 3 cm.)

The chronology established for LU-6 and LU-7, on the basis of several independent techniques with reproducible results, provides a minimum age of ~430 ka for the SH human fossils, which is some 100 ka younger than previously reported (37). With this new age, the SH hominins are now the oldest reliably dated hominins to show clear Neandertal apomorphies. Notably, the improved chronology for the SH assemblage is compatible with the latest dental and genetic evidence for Middle Pleistocene evolutionary divergences (38, 39) and enables us to state with certainty that the modern human/Neandertal most recent common ancestor dates to sometime before ~430 ka (pre–MIS 11).                   

The considerably enlarged SH cranial sample is morphologically quite homogeneous. In addition to some plesiomorphic traits in the cranial vault (such as the low position of the maximum cranial breadth), derived Neandertal traits are present in the midfacial projection, morphology of the supraorbital torus, and the glenoid cavity. Although the occipital morphology is not Neandertal-like, there is a flat supratoral surface that may be derived in the direction of the Neandertals. Finally, the SH mandibles and the dentition also show a derived Neandertal pattern, together with some distinctive dental features. In sum, the SH sample shows a constellation of derived Neandertal facial, dental, mandibular, and glenoid features that appears to represent a single functional masticatory complex. At the same time, the cranial vault lacks Neandertal specializations. This mosaic pattern fits the prediction of the accretion model for the first stage of Neandertal evolution.

Concerning the taxonomy of the SH fossils, we have long maintained that the SH hominins are members of the Neandertal lineage (16, 40). Based on the cranial evidence, we have proposed that the SH fossils, as well as the rest of the European early and middle Middle Pleistocene specimens, should be assigned to the species Homo heidelbergensis defined in a broad sense to include fossils with a generally more primitive morphology than the late Middle Pleistocene and Late Pleistocene Neandertals, even if they exhibit some derived Neandertal traits (19). However, the difficulty with identifying derived Neandertal features in the Mauer mandible, the type specimen of H. heidelbergensis, contrasts strongly with the presence of numerous Neandertal apomorphies in the SH mandibles (41). On this basis, we suggest that the SH sample be removed from the H. heidelbergensis hypodigm. An alternative view of H. heidelbergensis is as a Middle Pleistocene taxon that includes only fossils that lack any Neandertal apomorphies, and, in this restricted sense, the species is seen as the stem group for Neandertals and modern humans (7).

In addition, the new evidence presented here based on cranial morphology confirms that the SH population differs from some other European MPHs, such as Ceprano and Arago, that do not exhibit the suite of derived Neandertal features seen in SH. Thus, more than one evolutionary lineage appears to have coexisted during the European Middle Pleistocene (42), with that represented by the SH sample being phylogenetically closer (i.e., a sister group) to the Neandertals.

Some authors have, indeed, recommended that the SH fossils be included in H. neanderthalensis (5, 7) as early members of this evolutionary lineage. However, although we agree that the SH hominins are members of the Neandertal clade, the present analysis has shown that they differ from Neandertals in several cranial regions that are considered taxonomically diagnostic of H. neanderthalensis. We argue that the SH p-deme is sufficiently different from that of H. neanderthalensis so as to be considered a separate taxon. Whether this difference should be recognized on the specific or subspecific level is currently an open question.

Related to this, a nearly complete mitochondrial genome recently sequenced from a SH femur (43) groups with two Denisovan individuals rather than with Neandertals. This surprising result might seem to contradict our morphological interpretation of the SH population belonging to the Neandertal clade. However, based on analysis of their nuclear genome, the Denisovans are considered a sister group to Neandertals (44). It is possible that two deeply divergent mitochondrial DNA (mtDNA) lineages coexisted in the SH population, one that later characterizes the Denisovans and another (as yet undocumented) mtDNA lineage that became fixed in Neandertals. Alternatively, it is possible that gene flow from another hominin population (not belonging to the Neandertal clade) brought the Denisova-like mtDNA into the SH population or its ancestors. The latter scenario would imply that two different hominin clades (the Neandertal clade and another more primitive clade) coexisted in Europe for some time, an interpretation that is not contradicted by the fossil evidence. Retrieving additional mitochondrial or nuclear DNA sequences from the SH sample may help clarify our understanding.

It is important to underline that the morphology of the SH crania, mandibles, and teeth is very constant for those features that have been considered taxonomically relevant, without polymorphisms or different trait combinations. This finding was not a foregone conclusion, because the SH variation could have encompassed the range of variation found among different European fossils that are broadly contemporaneous. However, it is clear that there is more variation between demes in the European mid Middle Pleistocene than there is within the SH deme. The morphological variability among a single p-deme can be used to distinguish between anagenetic (linear) or cladogenetic (branching) patterns of evolution. The former implies that the population as a whole (of which any particular p-deme is but one component) evolves in a similar direction throughout its geographic range, and that the individual p-demes show a large degree of intrademe morphological variation. In contrast, the latter is more consistent with the cladogenetic model and implies that evolutionary change occurs via sorting between p-demes, which individually show little intrademe variation.

Although the accretion model is potentially consistent with either an anagenetic or cladogenetic mode of evolution, our morphological analysis of the SH sample fits the latter more closely. Moreover, the scenario of several demographic crashes influenced by climatic crisis throughout the European Middle Pleistocene would produce p-deme sorting, with extinction of some populations and replacement by others (5). The presence in the SH skulls of Neandertal-derived regions that can be functionally related in modules, together with others that remain primitive, combined with the pre-MIS 11 age of the sample, confirms the accretion model of Neandertal origins. Finally, the finding that these derived Neandertal features are functionally related with the masticatory complex suggests that the origin of the Neandertal clade coincides with a masticatory specialization.

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