Metric and morphological comparison between the Arago (France) and Atapuerca-Sima de los Huesos (Spain) dental samples, and the origin of Neanderthals
Introduction
Over the years, the interpretation of the European Pleistocene fossil record has increasingly captured the attention of many specialists. This interpretation has undergone substantial changes as the number of human fossils has increased, the dating of many sites has improved, and new lines of research have been opened, such as palaeogenetics. Therefore, presenting an exhaustive history of research on human evolution in Europe during the Pleistocene is beyond the scope of this work. It is nonetheless interesting, and relevant to our present discussion to refer back to the main hypotheses that were proposed during the second half of the twentieth century, and during this century, on the origins of the Neanderthals.
The so-called presapiens theory, proposed by Vallois (1954), attempted to show a primary bifurcation into two distinct lines: “Neanderthal” and “sapiens”. This hypothesis was criticized by Howell (1960), who did not find significant differences between Steinheim and Swanscombe, two key specimens in the presapiens theory. Moreover, Howell (1960) was very clear in his separation of the Pleistocene populations found in the European fossil record and those found in eastern Asia and northern Africa, which today have been attributed by many to H. erectus. Howell (1960) divided temporally the European hominin fossil record in two phases: “(1) the pre- Great Interglacial range (early Middle Pleistocene) and (2) the Great Interglacial and subsequent early phase of the Penultimate Glacial range (later Middle Pleistocene)”. After his detailed study of the limited fossil record of that time, Howell (1960, p. 223) conclude that “ The evidence would suggest that two distinctive hominid lineages were differentiated within the Middle Pleistocene, one represented by eastern Asian and northwest African populations, and the other by European populations”.
Aguirre et al. (1976) and Aguirre and de Lumley (1977) studied the fossil hominins recovered from the Atapuerca-SH site. These authors included these fossils alongside those of Arago and Mauer in the so-called ‘Anteneanderthal population’. This term, which has dominated the scientific literature for decades, alludes to the clear phylogenetic relationship between the human populations of the Middle Pleistocene and the Neanderthals of the Late Pleistocene. Aguirre and de Lumley (1977) were also not comfortable with the idea of including any other Pleistocene remains from Europe in the H. erectus taxon which, according to these authors, “should be restricted to the fossils from Java”. Nevertheless, the idea that anteneaderthals (or at least some of them) represent a particular lineage of H. erectus has persisted for decades (e.g. Jelinek, 1986; De Lumley, 2015 , but see Howell, 1986).
Although Thoma (1966) revived the presapiens hypothesis, the idea that in Europe there was a great biodiversity of human populations, and all of them were related to Neanderthals, appears clearly in the review carried out by Howells (1980). In the same sense, Bräuer (1984) presented evidence against the hypothesis of the origin of H. sapiens in Europe. This author proposed the “Afro-European sapiens hypothesis” and considered that all European Middle Pleistocene specimens represent a very variable Anteneanderthal population. According to this hypothesis, a bottleneck of this population was the origin of the so-called preneanderthals during the late Middle Pleistocene.
In their classic report, Cook et al. (1982) reviewed the ups and downs associated with dating Middle Pleistocene European sites comprising human remains. A lack of dates, or unreliable dates, are two of the main problems when interpreting the fossil record, although geochronological methods have been progressively improving through time and are currently being applied to many of these sites (e.g., Arsuaga et al., 2014; Daura et al., 2017; Falguères et al., 2004; Wagner et al., 2010). Today, the temporal framework is much more precise, but still requires improvement.
A general consensus on the origin of Neanderthals was reached during the 1980s and at the beginning of the 1990s (e.g. Arsuaga et al., 1993; Arsuaga et al., 1996; Hublin, 1988a; Hublin, 1990; Stringer, 1993). Hublin 1988a, 1988b considered that all European Middle Pleistocene fossils were related to Neanderthals, except Mauer, Vértesszöllös, and Bilzingsleben, although, according to his later works (Hublin, 1996), the possible absence of Neanderthal features in these specimens was not a criterion in itself to exclude them from the Neanderthal lineage. On this matter, it is interesting to mention that other authors have noted some Neanderthal features in the Mauer mandible, the holotype of H. heidelbergensis (Bermúdez de Castro et al., 2016; Mounier et al., 2009; Rosas and Bermúdez de Castro, 1998). The notion that European Middle Pleistocene hominins are distinct from those included in the H. erectus species led Stringer (1983, 1985) to postulate that specimens like those from Mauer, Vérteszöllös, Bilzingsleben, Arago, and Petralona, together with Broken Hill, Bodo, and Dali would represent the stem species (H. heidelbergensis) for Neanderthals and modern humans. This hypothesis was further developed by other colleagues (e.g. Rightmire, 1996; Rightmire, 1998; Tattersall, 1996). Arsuaga et al. (1997a) also included the SH hominins within this species. However, these last authors believe that H. heidelbergensis ought to be considered as an exclusive European chronospecies of the Neanderthal lineage. Later Arsuaga et al. (2014) left the SH hominins out of the H. heidelbergesis species, particularly because of the lack of cranial features like those found in other European Middle Pleistocene fossils, such as Ceprano (see below) and Arago, and the clear differences between the Mauer and the SH mandibular samples. The high degree of morphological diversity in the European Middle Pleistocene fossil record had begun to suggest a more complex view, especially after the discovery of the Ceprano calvaria (Ascenzi et al., 1996), the Mala Balanica mandible (Roksandic et al., 2011), and the Aroeira 3 cranium (Daura et al., 2017).
The Ceprano calvaria was first included in H. erectus, given its primitive morphology and its presumed early Pleistocene chronology (Ascenzi et al., 1996). However, new dating points provided an age range between 0.43 and 0.38 million years ago (Ma) (Manzi et al, 2010). Given this age and the observation that the morphology of the specimen has no equivalent in Europe, its taxonomic status remains controversial. This specimen has been also included in H. cepranensis (Mallegni et al., 2003), whereas new analyses led Mounier et al. (2011) and Manzi (2016) to initially include the Ceprano calvaria in the H. heidelbergensis species. The Mala Balanica mandibular fragment lacks Neanderthal features, and has been described as Homo sp (Roksandic et al., 2011). This specimen has been dated to the Middle Pleistocene (Rink et al., 2013). The Aroeira 3 cranium shows an interesting combination of cranial features present in the Atapuerca-SH, Arago, and Ceprano specimens, thus confirming the complexity that lies behind the interpretation of the European Middle Pleistocene fossil record (Daura et al., 2017). Finally, the analysis of the impressive cranial sample recovered from the SH hominins (Arsuaga et al., 2014) confirms the remarkable differences between these hominins and other European Middle Pleistocene specimens. This fact again drives the idea of the coexistence in Europe of more than one hominin lineage during this period (Tattersall, 2011; Stringer, 2012).
As noted above, it is clear that the significant morphological diversity of the European Middle Pleistocene fossil record cannot be avoided when researching human evolution. The complex physical geography, biogeography, and palaeoclimatology of the relatively small European continent may have played an important role in the demographic distribution and interaction of these Pleistocene populations. These factors may have given rise to different genetic processes including drift, founder effect, directional adaptation and hybridization (Daura et al., 2017; Dennell et al., 2011; MacDonald et al., 2012; Roksandic et al., 2011). Furthermore, the idea that different waves of populations arrived into Europe during the Pleistocene cannot be discarded (Bermúdez de Castro et al., 2016).
Tooth morphology has been considered to be highly heritable, selectively neutral, and evolutionary conservative, thus providing an excellent proxy for neutral genetic data (Hillson, 1996; Scott and Turner, 1997). In a recent study, Rathmann et al. (2017) have confirmed that dental phenotypic data (metric and no-metric traits) can be used as proxies for neutral genomic data in studies of population relatedness. Therefore, our aim is to compare the dental morphology of two important, geographically close, and approximately contemporaneous Middle Pleistocene hominin samples: Arago and Atapuerca-SH. We will evaluate and discuss the meaning of the possible similarities and differences between these two samples. Our null hypothesis is that, given the temporal and geographic proximity of the Arago and Atapuerca-SH sites, the differences noted between these two dental hominin samples are not significant. Thus, the Arago and Atapuerca-SH hominins may belong to the same biological population.
Section snippets
The Arago and Atapuerca-SH sites
The Caune de l’Arago (southern France) is a key site for the understanding of human evolution in Europe during the Middle Pleistocene. The sedimentary fill of the cave was assigned to this period on the basis of the mammalian fauna found within it (Chaline, 1981; Crégut, 1980; Guérin, 1981). The Middle Stratigraphical Complex of the Arago site includes, from bottom to top, four geological Units: I, II, III, and IV (De Lumley et al., 2015). Most human fossil remains have been recovered from Unit
Material and methods
The SH dental sample includes 530 permanent teeth (Table 1), whereas the Arago dental sample comprises 61 permanent teeth (Table 1). Details about the composition of the SH sample can be found in Martinón-Torres et al. (2012). The Arago sample analized in this report comprises 21 upper and 39 lower permanent specimens and 39 lower specimens. The Arago 2 mandible preserves in-situ the right M1 and the left M1, M2 and M3. The Arago 13 left hemimandible preserves in-situ the P3-M3 sequence. The
Upper central incisors (I1)
All the I1s from SH show some degree of a shovel shape, although it is generally moderate (ASUDAS grades 1 to 4). The large, round basal eminence occupies one to two-thirds of the lingual surface, thus reducing the lingual fossa associated with the shovel shape. The basal eminence takes the form of a moderate tuberculum dentale (grade 3) in the shape of enamel folds and depressions in only 25% of the specimens (Martinón-Torres et al., 2012). From the occlusal view the lingual convexity is
Comparative assessment
In this report we have carried out a comparative study of the Arago and Atapuerca-SH hominin dental samples. The distance between the two sites is only 630 kilometres as the crow flies, and the stratigraphic levels comprising hominin remains are roughly contemporaneous. Of course, the Pyrenees was one of the multiple geographical barriers of the European continent. The Pyrenees slowed down the passage of species between northern Europe and the Iberian Peninsula. But it is important to note that
Concluding remarks
The comparison between the Arago and SH dental samples is consistent with the hypothesis that more than one hominin lineage lived in Europe during the Middle Pleistocene. Given the geographic and temporal proximity between these two sites, we cannot suggest isolation, genetic drift, founder effect, or directional adaptation to explain the differences observed between Arago and SH. However, the two dental assemblages share the Eurasian pattern of anterior and posterior dentition previously
Acknowledgements
We are especially grateful to Profs Henry and Marie Antoinette de Lumley, directors of the Arago excavations and research, for giving us permission to study the Arago dental sample on three separate occasions, and for allowing us to take photographs of the specimens. Their friendly hospitality means a lot to us. We are also very grateful to Drs Avi Gopher and Ran Barkai, directors of the Qesem archaeological excavations at the Qesem site, and to Prof. Israel Hershkovitz, for their kindness and
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