Comment on ‘Krapina atlases suggest a high prevalence of anatomical variations in the first cervical vertebra of Neanderthals’

Abstract

A review of the observation of an anterior cleft on the atlas of a Neanderthal from Krapina.

We read with interest the article published in the Journal of Anatomy by Palancar et al. (2020), about anatomical variations in the first cervical vertebra of the Krapina Neanderthals. This is a welcomed contribution to furthering our understanding of developmental and congenital anomalies in hominins. While the article provides detailed and sustained arguments for its general interpretations and conclusions, we believe there is one correction that needs to be done. Specifically, Palancar et al. (2020) state that Krapina 99 (Kr.99) ‘is a right lateral mass of an adult atlas’, with a completely fused transverse process ‘without any sign of active ossification’, and with ‘a non‐fused anterior atlas arch (anterior atlas arch cleft)’ (Palancar et al., 2020: 3). The authors continue the description of the anterior synchondrosis in Kr.99 as exhibiting ‘the presence of a porous‐like surface quite similar to that described previously in the literature (Ríos 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 Ríos 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.’ (Palancar et al., 2020: 3).

Based on the graphic information provided by Palancar et al. (2020), it is our opinion that Kr.99 represents a juvenile atlas with an unfused anterior synchondrosis (AS), and not an adult atlas with an anterior cleft. Our opinion is based on the following observations/considerations:

1. Although the transverse process is described by Palancar et al. (2020) as ‘completely fused, without any sign of active ossification’, this is inconsistent with the observation of Palancar et al.'s (2020) Figure 2A, B, and D which illustrates the transverse process as exhibiting notched edges, and a tenuous billowing surface pattern, while the generally smooth end of the transverse process, typical of mature vertebrae, is absent. These observations are more akin to a vertebra in the last stages of maturation, where the secondary ossification centre of the transverse process has not yet commenced fusion. By modern human standards, lack of fusion of this small epiphysis indicates an age under 18 years old (Cardoso and Rios, 2011, see Fig. S3 therein, plates A and B).

2. The macroscopic aspect of the presumed defect of the anterior arch (Figure 2D and E, Palancar et al., 2020) presents the partially flattened surface and well‐defined perimeter of an anterior synchondrosis (AS) in the last stages before fusion with the anterior arch. For comparative purposes, we provide an ontogenetic series of the normal shape changes of the left AS in Figure 1. The clear delimitation of the AS in Kr.99 (Figure 2E and Figure 3B, Palancar et al., 2020) is quite similar to the AS of case E, indicating the presence of a non‐fused AS. While the contour of the superior articular facet in Kr.99 seems to be less well marked than in the Kr.98 adult atlas, suggesting that the individual is not fully mature, Palancar et al. (2020) might have been confused by the overall mature morphology of Kr.99. The shape and location of the AS might have also confused the interpretation about the maturity status of Kr.99. As described by Cunningham et al. (2016: 202), generally ‘the line of union between the anterior arch and a lateral mass passes across the anterior portions of the superior articular facet’. In the case of Kr.99 and from the images provided by Palancar et al. (2020), the line of union seems to be located in a more anterior position, either just in the border of, or 1‐2 mm beyond, the superior articular facet, as expected if Kr.99 was not fully adult. We also have to bear in mind that ossification at the AS presents a high level of normal variation (Piatt and Grissom, 2011; Karwacki and Schneider, 2012). For instance, an atlas with a similarly shaped AS to Kr.99 is shown in Cunningham et al. (2016, Figure 7‐28C: 203), albeit at an earlier developmental stage. The juvenile atlas that we show in Figure 1e also presents the AS at the end of a short process. Furthermore, the small anterior process that harbours the AS in Kr.99 is shorter than the same process in the atlases of two Neanderthal individuals from El Sidrón diagnosed with an anterior cleft. In the case of El Sidrón, both anterior processes extend for more than 1 cm beyond the anteriormost point of the superior articular surface, approaching the sagittal plane (see Figure 2A in Ríos et al., 2015; and Supplementary Fig. S2 in Ríos et al., 2019). In Figure 2, we show the atlas of a juvenile skeleton with a sagittal, unfused, AS. In this case, there was no development of the anterior ossification centre (anterior arch), and the anterior arch and the single AS were formed by ossification extending from the lateral masses towards the sagittal plane. The location of the AS in Kr.99, immediately anterior to the superior articular facet and away from the sagittal plane, suggests the presence of an unfused anterior arch and not of a cleft.

3. When the authors state ‘a porous‐like surface quite similar to that described previously in the literature (Ríos et al., 2015; Sanchis‐Gimeno et al., 2017) that support the diagnosis of anatomical variations’, they misinterpret the observations and reasoning of the original article (Ríos et al., 2015). Ríos et al. (2015) described this porous‐like surface, formed by numerous and small pore‐like structures, as typical of the normal synchondrosis (see Figure 5 in Ríos et al., 2015). And it was not the presence, but precisely the absence of this porous‐like surface together with continuity of cortical bone what indicated that there was no actual AS in the atlas of El Sidrón Neanderthal SD‐1094. It is the absence of a porous‐like surface typical of the synchondrosis what would exclude a normal‐for‐age lack of fusion of the AS, lending support to the presence of a congenital cleft. Although this porous‐like surface was originally observed with environmental scanning electron microscope, it might be distinguished from cortical bone at plain sight (Ríos et al., 2015, 2019). For instance, in Figure 2b it can be observed the difference in texture between the cortical bone (C) and the porous‐like surface (P), indicating that the gap in this atlas should be considered an unfused AS. Although difficult to observe in Figure 2E and 3B from Palancar et al. (2020) due to image resolution, the authors noted the presence of this porous‐like surface in Kr.99, which would indicate the presence of an unfused AS.

FIGURE 1.

An ontogenetic series of the shape changes at the anterior synchondrosis (AS) in five cases with unfused AS. For each case, from left to right, we present posterior medial, medial and anterior medial views of the AS. In (a and b), the AS presents a pointed shape, and its surface is not differentiated from the condylar surface. A more differentiated and delimited AS can be observed in (c), with a defined vertical orientation and more angled contour. Further delimitation of the AS can be observed in (d), with a well‐defined contour along its perimeter, with a sharp border at its anterior aspect. In (e), we observe the well‐defined contour of the AS and the beginning of bone activity in the inferior half of the contour, observable as a flange, absent in the superior half and which represents the phase immediately prior to beginning of fusion. White bars: 5 mm

FIGURE 2.

Superior view of the atlas of a juvenile skeleton. (a) Superior view, where the single anterior synchondrosis marked by the asterisk can be observed. The double arrow indicates the length of the process harbouring the synchondrosis, from the superior articular facet towards the sagittal plane. (b) Detail of the synchondrosis, where the difference in appearance between the cortical bone (marked by a C), and the porous‐like surface of the synchondrosis can be observed. White bar: 2 mm

In the context of recent findings about skeletal anomalies in Pleistocene hominins (Ríos et al., 2015, 2019; Gómez‐Olivencia et al., 2018; Rmoutilová et al., 2020), and as summarized by Trinkaus (2018), the review of known individuals or collections may provide insights into aspects of survival, stress, consanguinity and mortuary behaviour among these foraging populations. The study by Palancar et al. (2020) is another step in that direction, but in our opinion the evidence presented by the authors does not support the consideration of Kr.99 as a Neanderthal adult atlas vertebra with an anterior cleft. This Neanderthal specimen probably corresponds to a late juvenile atlas vertebra with a non‐fused anterior synchondrosis.

AUTHOR CONTRIBUTIONS

L.R designed the research. L.R. and H.C contributed to acquisition, analysis and interpretation of data. L.R. and H.C. contributed to drafting, revision and approval of the manuscript.