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. 2020 May 21;237(3):579–586. doi: 10.1111/joa.13215

Krapina atlases suggest a high prevalence of anatomical variations in the first cervical vertebra of Neanderthals

Carlos A Palancar 1,2,3, Daniel García‐Martínez 1,4, Davorka Radovčić 5, Susanna Llidó 6, Federico Mata‐Escolano 6, Markus Bastir 1,6, Juan Alberto Sanchis‐Gimeno 6,✉
PMCID: PMC7476204  PMID: 32436615

Abstract

The first cervical vertebra, atlas, and its anatomical variants have been widely studied in Homo sapiens. However, in Neanderthals, the presence of anatomical variants of the atlas has been very little studied until very recently. Only the Neanderthal group from the El Sidrón site (Spain) has been analysed with regard to the anatomical variants of the atlas. A high prevalence of anatomical variants has been described in this sample, which points to low genetic diversity in this Neanderthal group. Even so, the high prevalence of anatomical variations detected in El Sidrón Neanderthal atlases needs to be confirmed by analysing more Neanderthal remains. In this context, we analysed the possible presence of anatomical variants in the three Neanderthal atlases recovered from the Krapina site (Croatia) within the Neanderthal lineage. Two of the three Krapina atlases presented anatomical variations. One atlas (Krapina 98) had an unclosed transverse foramen and the other (Krapina 99) presented a non‐fused anterior atlas arch. Moreover, an extended review of the bibliography also showed these anatomical variations in other Middle and Upper Pleistocene hominins, leading us to hypothesise that anatomical variations of the atlas had a higher prevalence in extinct hominins than in modern humans.

Keywords: anatomical variants, atlas, Krapina, Neanderthal

Krapina atlases confirm the high prevalence of C1 anatomical variations shown by the El Sidrón Neanderthal sample. The high prevalence of anatomical variations led us to hypothesize that Middle and Upper Pleistocene hominins would have a large degree of inbreeding, as several individuals seem to present anatomical variations of the atlas, a feature that seems to be related to low genetic diversity.

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1. Introduction

The atlas (C1) is an atypical cervical vertebra, both anatomically and functionally (Scheuer and Black, 2000). It consists of an anterior and posterior arch, two lateral masses and the neural canal (Drake et al. 2010; White et al. 2011). These lateral masses consist of a transverse process and both superior and inferior articular facets. The superior facets join the occipital condyles and the inferior facets join the axis (second cervical vertebra, C2). The transverse processes have a transverse foramen for the vertebral artery. The atlas lacks a vertebral body; in its hypothetical position, the fovea dentis joins the dens of the axis. The lateral masses in their medial margin have tubercles for the insertion of the transverse ligament, which is implicated in the articulation of the dens of the axis and the atlas (Drake et al. 2010; White et al. 2011).

It is known that, in Homo sapiens, the atlas ossifies from three primary centres of ossification. One in each lateral mass, posterior to the articular pillar and active from the seventh week of prenatal life, and one in the anterior arch, active from the first year of life (Scheuer and Black, 2000). The transverse process is formed by the fusion of the thick posterior bar, as a consequence of the lateral spread of the centre of ossification of the lateral mass, with a thinner anterior bar developed from the ventrolateral edge of the articular pillar, between the third and fourth year of life (Scheuer and Black, 2000). The anterior centre of ossification spreads laterally to form an identifiable anterior arch in the third/fourth year of life. The anterior arch fuses each lateral mass at the neurocentral junction at the age of 5 or 6 years. This neurocentral junction is located across the anterior portions of the superior articular facet (Scheuer and Black, 2000). In sum, the normal atlas in adults is ring‐like and consists of an anterior arch and a posterior arch, which both unite the two lateral masses. The anterior arch forms approximately one‐fifth of the ring, while the posterior arch forms approximately two‐fifths of the circumference of the ring. Both left and right transverse foramina are closed, and both anterior and posterior arches are fused.

It is important to note that the presence and/or prevalence of different anatomical variants has been related to several diseases, low genetic diversity and inbreeding (Klimo et al. 2003; Cakmak et al. 2005; Billman and Le Minor, 2009; Elliott and Tanweer, 2014; Fuhrhop et al. 2015; Ríos et al. 2015; Pękala et al. 2017; Pękala et al. 2018; Ríos et al. 2019). Indeed, a familial association has been found in the presence of anatomical variants of the atlas in H. sapiens (Currarino et al. 1994; Al Kaissi et al. 2007). While anatomical variants of the atlas, such as anterior and posterior arch defects, unclosed transverse foramen (UTF), arcuate foramen (AF) or retrotransverse foramen (RTF), have been fully studied in H. sapiens (Currarino et al. 1994; Le Minor, 1997; Klimo et al. 2003; Sanchis‐Gimeno and Aparicio, 2011; Sanchis‐Gimeno et al. 2014; Unlu et al. 2016; Pękala et al. 2017; Ríos et al. 2017; Tambawala et al. 2017; Pękala et al. 2018; Sanchis‐Gimeno et al. 2018a; 2018b), little has been published about the presence of anatomical variants of the atlas in a Neanderthal population. Nevertheless, and in spite of the low number of Neanderthal atlases recovered to date, the presence of anatomical variations, such as non‐fused arches, has been described in the El Sidrón (Asturias, Northern Spain) Neanderthal group (Ríos et al. 2015). As a result, the anatomical variations of the atlas observed in the El Sidrón Neanderthal group should be confirmed by analysing more Neanderthal remains.

In this context, the Krapina (Croatia) Neanderthal sample is potentially a good comparative group, as they share common features with the El Sidrón sample. The site of Krapina is a 12‐m high rock shelter located on Hušnjakovo hill in the town of Krapina, 55 km north of Zagreb, Croatia (Trinkaus, 1985; Radovčić, 1988). Pleistocene deposits were discovered there in 1895, and were excavated between 1899 and 1905 by D. Gorjanović‐Kramberger, who recovered a great number of fossils (Trinkaus, 1985; Russell, 1987). More than 850 bones and bone fragments from several Neanderthal individuals were found to be associated with Middle Palaeolithic industry (Gorjanović‐Kramberger, 1906; Radovčić et al. 1988) which makes the Krapina sample the largest of Neanderthal remains from one single site (Trinkaus, 1985). The dating of the fossils has been estimated at 130 ± 10 kyr by electron spin resonance and U‐series (Rink et al. 1995). A large number of axial bone remains have been found among the human skeletal remains from Krapina. In this context, ribs have been partially studied (García‐Martínez et al. 2018) while a detailed study of the cervical vertebrae was carried out by Gorjanović‐Kramberger (1929).

We endeavoured to analyse the possible presence of anatomical variants in the Neanderthal atlases of Krapina, a sample that probably represents closely related individuals which may well be attributable to inbreeding, and probably represents a population (paleodeme) of Neanderthals (Gorjanović‐Kramberger, 1906; Trinkaus, 1985; Bocquet‐Appel and Arsuaga, 1999). Several studies suggest high frequencies of anomalies in the Krapina sample in other anatomical regions such as the nasal and temporal bones and the premolars (Smith and Smith, 1986; Frayer, 1992a,b; Wolpoff, 1999); however, the Krapina atlases have not yet been analysed in this regard.

2. Materials and methods

2.1. Neanderthal atlases

A total of 22 bone fragments of cervical vertebrae were recovered at the Krapina site (Radovčić et al. 1988). Four of these fragments belonged to Neanderthal atlases, which are the object of the present study. These atlas fragments were: Krapina 98 (Kr.98), an anterior fragment with both lateral masses and the anterior arch; Krapina 99 (Kr.99), a complete right lateral mass; Krapina 100 (Kr.100), a complete left lateral mass; and Krapina 101 (Kr.101), an almost complete posterior arch which fits with Krapina 100. As the Krapina sample exhibits a high level of fragmentation and disassociation (Trinkaus, 1985; Russell, 1987; Radovčić et al. 1988), it was not possible to determine the age and sex of these vertebrae, but Radovčić et al. (1988) catalogued these atlases as being those of adults.

2.2. Identification of anatomical variants

Krapina atlases were assessed by researchers and the presence of anatomical variants was verified by each researcher independently. After visual inspection, the atlases were examined under a microscope, and radiographs (Kricun et al. 1999) were used to rule out the presence of any fractures that could superficially mimic an anatomical variant (Sanchis‐Gimeno et al. 2014). When cortical bone was present in the region under study with no signs of osteogenic reaction, a fracture had to be ruled out, and the presence of an anatomical variant was suspected (Sanchis‐Gimeno et al. 2014).

3. Results

Krapina 98 (Fig. 1) is an anterior fragment of an adult atlas. It only preserves the anterior arch, both lateral masses and the right transverse process, so the posterior arch and the left transverse process are missing. The tuberosities for the insertion of the transverse ligament are weakly developed and the anterior tubercle is prominent and oriented caudally, as seen in other Neanderthals (Gómez‐Olivencia et al. 2013). However, in Kr.98, this anterior tubercle is slightly deviated towards the right. The fovea dentis is wide and the lateral masses are not symmetrical because the left lateral mass is more laterally oriented while the right lateral mass is more medially oriented. The superior articular facets show a slight invagination in the medial margin. The right superior articular facet is slightly larger than the left. The inferior articular facets are elongated dorsoventrally. Nevertheless, the analysis of the right transverse foramen revealed that Kr.98 presents an anatomical variation: a UTF.

Fig. 1.

Fig. 1

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Krapina 98 first cervical vertebra (C1, atlas) fragment. The white asterisk marks the unclosed transverse foramen (UTF). (A) Inferior view. (B) Superior view. (C) Anterior view. (D) Radiograph of Krapina 98; (E) detailed view of the UTF; the photo was taken supero‐anteriorly.

Krapina 99 (Fig. 2) is a right lateral mass of an adult atlas. Both superior and inferior articular facets, the transverse process and its transverse foramen have been preserved. The tuberosity for the insertion of the transverse ligament is also weakly developed. The transverse process is completely fused, without any sign of active ossification. The posterior arch is broken in the dorsal margin of the lateral mass. The anterior arch presents no evidence of fracture, the cortical bone is present in the anterior margin and the lateral crest of the fovea dentis is present. As a result, Kr.99 presents an anatomical variation: a non‐fused anterior atlas arch (anterior atlas arch cleft).

Fig. 2.

Fig. 2

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Krapina 99 first cervical vertebra (C1, atlas) fragment. The white asterisk marks the anterior cleft. (A) Inferior view. (B) Superior view. (C) Radiograph of Krapina 99. (D) Detailed view of the defect in the anterior arch; the photo was taken from the front. (E) Detailed view of the anterior arch defect; the photo was taken from medial view.

The stereomicroscopy study (Fig. 3) displayed regular and smooth edges without sclerosis and no callus formation or residual cortical deformity in both Kr.98 and Kr.99. We also observed the presence of a porous‐like surface quite similar to that described previously in the literature (Rios et al. 2015; Sanchis‐Gimeno et al. 2017) that support the diagnosis of anatomical variations. In addition, and in line with the observations made by Rios et al. (2015) in El Sidrón Neanderthals, the surface of the synchondrosis of Kr.99 was uniform. It also supports the diagnosis of a non‐fusion of the anterior atlas arch (anterior atlas cleft) in Kr.99.

Fig. 3.

Fig. 3

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10x stereomicroscopy study of the region of interest of Krapina 98 (A) and Krapina 99 (B).

Krapina 100 (Fig. 4) is a complete left lateral mass that fits with Kr.101, which is an almost complete posterior arch. Together they form an adult atlas which only lacks the right lateral mass and the anterior arch. As a result, we will refer to it as Kr.100 in the present paper. Its tuberosity for the insertion of the transverse ligament is also weakly developed. The groove for the left vertebral artery is well marked and the posterior tubercle is present. The left transverse process is completely fused. Nevertheless, as Kr.100 presents some taphonomic damage and lacks the right lateral mass and the anterior arch, and although the posterior right arch seems to be compatible with a posterior atlas arch defect classified as Type B according to the classification by Currarino et al. (1994), we prefer to take a more conservative view and refer to it as a normal atlas, pending future more complex analysis.

Fig. 4.

Fig. 4

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Superior view of Krapina 100 first cervical vertebra (C1, atlas) fragment.

4. Discussion

We have analysed three adult Neanderthal atlases and have found a UTF in Kr.98 and a non‐fused anterior atlas arch (or anterior cleft) in Kr.99, and we have taken a conservative approach to Kr.100 and have opted to assign Kr.100 as a normal atlas. As a result, and with the conservative approach we took in the analysis of the atlases, we have found that two out of three Neanderthal atlases presented anatomical variations.

As commented, we found a UTF in Kr.98. The UTF is an anatomical variant of the atlas caused by the absence of the anterior, thinner bar, resulting in a new structure that can be considered as a transverse vertebral notch (Travan et al. 2015; Sanchis‐Gimeno et al. 2018b) which is found in approximately 8% to 10% (Billmann and Le Minor, 2009; Travan et al. 2015; Sanchis‐Gimeno et al. 2018b) of H. sapiens.

We have also found another anatomical variation, which appears to be a non‐fused anterior arch (anterior atlas arch cleft), in Kr.99. Non‐fusions of the anterior atlas arch are a rare anomaly consisting of the developmental failure of chondrogenesis (Kwon et al. 2009). An anterior arch non‐fusion (or anterior atlas arch cleft) may occur in two different ways: the absence of the anterior ossification centre, resulting in the lateral masses not fusing anteriorly, or the non‐fusion between the anterior tubercle and the ossification centre of the anterior arch (Kwon et al. 2009). The anterior cleft is observed in a maximum of 0.1% (Kwon et al. 2009; Hummel and de Groot, 2013) of H. sapiens and may be associated with a posterior non‐fused atlas arch, resulting in the so‐called bipartite atlas (Gamble and Rinsky, 1985; Garg et al. 2004; Senoglu et al. 2007; Hummel and de Groot, 2013; Allam & Zhou 2015; Unlu et al. 2016). As Kr.99 lacks the posterior arch, we cannot confirm the presence of a posterior cleft or non‐fused posterior arch, but the literature reveals that the non‐fused posterior arch is present in up to approximately 4% of H. sapiens (Currarino et al. 1994; Senoglu et al. 2007; Sanchis‐Gimeno and Aparicio, 2011; Jin et al, 2014; Sanchis‐Gimeno et al. 2018b), and has been described in the El Sidrón Neanderthal group (Ríos et al. 2015). In addition, the El Sidrón Neanderthal group presents anterior atlas arch clefts as is the case in Kr.99. As our results agree with the findings obtained in the El Sidrón Neanderthal group (Ríos et al. 2015) these findings may suggest a generalized pattern of the high presence of anatomical variations in the Neanderthal atlases possibly related to inbreeding (Ríos et al. 2015; Ríos et al. 2019).

During the last decades, paleo‐geneticists have delved into the genetic diversity of the Neanderthal lineage. Krings et al. (2000) suggested that the genetic diversity of three Neanderthal mtDNAs, specifically the Feldhofer, Mezmaiskaya and Vindja individuals, was lower (3.73%) than that of chimpanzees (14.82%) and gorillas (18.57%), even though they inhabited a region much larger than those apes. This may indicate that they expanded from a small population. Later, LaLueza‐Fox et al. (2006) also proposed that, in spite of the broad geographic range, the El Sidrón, Feldhofer and Vindija Neanderthals may belong to the same Neanderthal lineage. However, based on other genetic evidence, Excoffier (2006) indicated that younger Neanderthal sequences are more similar to modern humans than older Neanderthal sequences, suggesting a potential Neanderthal‐modern human inbreeding, which did not exclude a low genetic diversity in Neanderthals. In 2011, Lalueza‐Fox et al. (2011) studied the genetic diversity of the El Sidrón Neanderthals, a group potentially associated with the same family group. They found that the El Sidrón mtDNA diversity was significantly lower than any random subsample of sequences from unrelated modern Europeans, suggesting that mtDNA genetic diversity was low within such Neanderthal groups.

This low genetic diversity that is very likely to be found in Neanderthal paleodemes, such as the ones from El Sidrón or from Krapina, also shows that low genetic diversity may play some role in the anatomical variations found in their skeletons. In this way, Ríos et al. (2015) found that two out of three atlases from the El Sidrón site had anatomical variants that present low frequencies in modern humans; indeed, and supporting the possible role of inbreeding, in H. sapiens a familial association has been found in the presence of anatomical variants of the atlas (Currarino et al. 1994; Al Kaissi et al. 2007). Those anatomical variations, along with other dental congenic anomalies in the canines, support the evidence of low genetic diversity in the El Sidrón group. It has also been suggested that the skeletal anomalies presented in the El Sidrón group support a role of inbreeding in Neanderthal extinction (Rios et al. 2019). In the same line, our results on the Krapina C1 vertebrae, also suggest a high frequency of anatomical variants that are usually found in low frequency in modern humans. However, while in the case of the El Sidrón site mtDNA has been studied, to the best of our knowledge, no such studies have been carried out to date on the Krapina remains.

Regarding the anatomical variations of the atlas in Neanderthals, Gómez‐Olivencia et al. (2018) observed an asymmetry in the posterior atlas arch of La Ferrassie 1 related to a persistent first intersegmental artery presence; a persistent first intersegmental artery has a prevalence of 4.7% in modern humans (Hong et al. 2008). In addition, Ríos et al. (2015, 2019) described anterior and posterior arch non‐fusions (anterior and posterior arch clefts) in the El Sidrón atlas remains. Regarding the El Sidrón group non‐fusions, and 'given the small sample of sufficiently complete Neanderthal C1s, it would be exceptional to find even two with such developmental non‐fusions' (See Supporting Information, p. 44 in Trinkaus, 2018). Nevertheless, another option that we suggest in view of the results obtained from the Krapina atlases is the hypothesis that it may not be an exceptional finding because there may have been a high prevalence of anatomical variants in Neanderthal atlases which would be in line with the observations of Trinkaus (2018) about developmental anomalies and abnormalities in Pleistocene people. In sum, it makes us wonder if the El Sidrón and Krapina results are more similar due to chance or whether they represent a regular Neanderthal pattern. In other words, is it possible that extinct hominins presented a high prevalence of anatomical variations in the atlas vertebra that has gone unnoticed? In order to answer this question, we have reviewed the literature to analyse the images presented in published articles and we address the possibility of five more atlas vertebrae of extinct hominins presenting anatomical variants of the atlas. Apart from the Krapina atlases shown in the present research and the atlases of the El Sidrón group (Ríos et al. 2015; Ríos et al. 2019), we consider that the atlas of Kebara 2 (fig 1 in Arensburg, 1991) and the atlas VC3 from the Sima de los Huesos site could also present a UTF (fig 2a in Gómez‐Olivencia et al. 2007).

Regarding other anatomical variants of the atlas, the AF consists of a complete osseous bridge over the groove for the vertebral artery (Sanchis‐Gimeno et al. 2018b), and it seems to be present in the VC7 fossil from the Sima de los Huesos site (Fig. 2d in Gómez‐Olivencia et al. 2007) and in the Neanderthal atlas of Shanidar 2 (Fig. 32b in Trinkaus, 2014). Although the existence of a bony arch in those atlases (Gómez‐Olivencia et al. 2007; Trinkaus, 2014) is mentioned, the fact that this is an anatomical variant, and therefore important, has been overlooked. The prevalence of AF in H. sapiens ranges from approximately 9% to 17% (Elliott and Tanweer, 2014; Pękala et al. 2017; Pękala et al. 2018), but more importantly, the vertebral artery may be compressed when the complete AF is present (Pękala et al. 2017), and the presence of an AF has been associated with clinical symptoms such as migraine, cervicogenic headache, vertigo, nausea, retro‐orbital pain, acute headache, neck pain, arm pain, shoulder pain, dissection of the vertebral artery, and so on (Wight et al. 1999; Cushing et al. 2001; Cakmak et al. 2005; Sabir et al. 2014; Ríos et al. 2017; Pękala et al. 2018). It is of special importance because the presence of the AF in Neanderthals may have had a clinical implication as it currently does in the case of H. sapiens. It is likely that something similar occurred regarding the non‐fusion of the posterior arches described in the El Sidrón group since in H. sapiens this non‐fusion has been associated with clinical symptoms that include chronic cervical pain, headache, a Lhermitte's sign, and cervical myelopathy (Klimo et al. 2003; Sagiuchi et al. 2006; Sabuncuoglu et al. 2011; Shah et al. 2017).

Furthermore, the VC3 atlas from the Sima de los Huesos site (Figure 2b in Gómez‐Olivencia et al. 2007) probably presents another anatomical variant, the RTF, which consists of an abnormal accessory foramen on the posterior root of the transverse process which is smaller than, and located behind, the transverse foramen (Le Minor, 1997; Paraskevas et al. 2005; Sanchis‐Gimeno et al. 2018a; Sanchis‐Gimeno et al. 2018b). The RTF contains the anastomotic vein connecting the venous sinuses above the posterior arch of the atlas (the sub‐occipital cavernous sinus) and below it (vertebral and the vertebral artery venous plexus) (Bodon et al. 2016), and its prevalence in H. sapiens is approximately 7.5% (Sanchis‐Gimeno et al. 2018a). Thus, the VC3 atlas from the Sima de los Huesos site could present two anatomical variants (UTF plus RTF), while researchers have found that only 1.8% of H. sapiens present a UTF plus an RTF in the same atlas vertebra (Sanchis‐Gimeno et al. 2018a). The possible anatomical variants in the extinct hominins that are mentioned in this study along with their prevalence in modern humans are summarized in Table 1.

Table 1.

Summary of the possible available evidence of atlas vertebra anatomical variants mentioned in this study, together with its prevalence in modern humans

Vertebra Anatomical variant Prevalence, %
SD‐636 Non‐fused anterior atlas arch (anterior atlas arch cleft)
SD‐1094 Non‐fused anterior atlas arch (anterior atlas arch cleft) 0.1
Kr.99 Non‐fused anterior atlas arch (anterior atlas arch cleft)
VC3 a Unclosed transverse foramen and retrotransverse foramen 1.8
SD‐1643 Non‐fused posterior atlas arch (posterior atlas arch cleft)
SD‐1725 Non‐fused posterior atlas arch (posterior atlas arch cleft) 4.0
SD‐2045 Non‐fused posterior atlas arch (posterior atlas arch cleft)
La Ferrassie 1 First intersegmental artery 4.7
VC3 a Retrotransverse foramen 7.5
Kebara 2 Unclosed transverse foramen
VC3 a Unclosed transverse foramen 8–10
Kr.98 Unclosed transverse foramen
VC7 Arcuate Foramen 9–17
Shanidar 2 Arcuate Foramen
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a

The anatomical variants of VC3 are presented individually and combined.

In sum, Krapina atlases seem to confirm the higher prevalence of anatomical variations in the first cervical vertebra of Neanderthals. The combination of the scarcity of atlases of extinct hominins and the presence of these anatomical variations lead us to hypothesize that these anatomical variations may not be exceptional findings and should be considered a consequence of a possible higher prevalence in extinct hominins than in H. sapiens caused by population inbreeding. We also recommend a careful analysis of the atlases of extinct hominins recovered to date, with a special focus on the detection of anatomical variations.

Conflict of interest

None declared.

Author contributions

Author contributions were as follows. Conceived and designed the experiments: C.A.P., J.A.S.‐G. Acquisition of data: C.A.P., D.G.‐M., D.R. Data analysis/interpretation: C.A.P., D.G.‐M., D.R., S.L., F.M.‐E., M.B., J.A.S.‐G. Drafting of the manuscript: C.A.P., J.A.S.‐G. Critical revision of the article: C.A.P., D.G.‐M., D.R., S.L., F.M.‐E., M.B., J.A.S.‐G. Approval of the article: C.A.P., D.G.‐M., D.R., S.L., F.M.‐E., M.B., J.A.S.‐G.

Acknowledgements

This research was funded by grants from the Ministry of Economy, Industry and Competitiveness (grant number: CGL2015‐63648‐P) and the University of Valencia (grant number: UV‐INV_AE18‐773873). D.G.M. is funded by the Juan de la Cierva Formación programme (FJCI‐2017‐32157), from the Spanish Ministry of Science, Innovation and Universities. We would like to thank Mr Francisco Javier Fernández‐Pérez, Ms Nicole Torres‐Tamayo, Mr Pedro Osborne‐Márquez and Ms Stephanie Lois‐Zlolniski, from MNCN‐CSIC, for their assistance in different phases of this research work.

Palancar CA, García‐Martínez D, Radovčić D, et al. Krapina atlases suggest a high prevalence of anatomical variations in the first cervical vertebra of Neanderthals. J. Anat. 2020;237:579–586. 10.1111/joa.13215

Data availability statement

The data that support the findings of this study are available from the corresponding author on reasonable request.

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Data Availability Statement

The data that support the findings of this study are available from the corresponding author on reasonable request.

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