Shape analysis of the StW 578 calotte from AUTHORS: Amélie Beaudet1,2,3 Jacovec Cavern, Gauteng (South Africa) Jean Dumoncel4 Jason L. Heaton5,6,7 Travis R. Pickering6,7,8 The fossiliferous deposits within the lower-lying Jacovec Cavern in the locality of Sterkfontein yielded Ronald J. Clarke6 Kristian J. Carlson6,9 valuable hominin remains, including the StW 578 specimen. Because StW 578 mainly preserves the Lunga Bam10 calotte, the taxonomic status of this specimen has been a matter of discussion. Within this context, Luc Van Hoorebeke11 Dominic Stratford2 here we employed high-resolution microtomography and a landmark-free registration method to explore taxonomically diagnostic features in the external surface of the StW 578 calotte. Our comparative sample AFFILIATIONS: included adult humans and common chimpanzees as well as one Australopithecus africanus specimen 1 Department of Archaeology, University of Cambridge, Cambridge, (Sts 5). We partially restored the StW 578 calotte digitally and compared it to extant specimens and Sts 5 United Kingdom using a landmark-free registration based on smooth and invertible surface deformation. Our comparative 2 School of Geography, Archaeology and Environmental Studies, University shape analysis reveals morphological differences with extant humans, especially in the frontal bones, of the Witwatersrand, Johannesburg, South Africa and with extant chimpanzees, as well as intriguing specificities in the morphology of the StW 578 parietal 3 Catalan Institute of Palaeontology bones. Lastly, our study suggests morphological proximity between StW 578 and Sts 5. Given the Miquel Crusafont, Autonomous University of Barcelona, Barcelona, intimate relationship between the brain and the braincase, as well as the integration of the hominin face Spain and neurocranium, we suggest that cranial vault shape differences between StW 578 and extant humans, 4 French National Centre for Scientific Research (CNRS), Paris, France if confirmed by further analyses, could be either explained by differences in brain surface morphology 5 Department of Biology, Birmingham- or in the face. Besides providing additional information about the morphology of the Jacovec calotte that Southern College, Birmingham, Alabama, USA will be useful in future taxonomic discussion, this study introduces a new protocol for the landmark-free 6 Evolutionary Studies Institute, analysis of fossil hominin cranial shape. University of the Witwatersrand, Johannesburg, South Africa Significance: 7 Plio-Pleistocene Palaeontology Section, Department of Vertebrates, • We provide further information on the enigmatic fossil specimen StW 578. Ditsong National Museum of Natural History, Pretoria, South Africa • We introduce a new approach for the morphological study of fossil hominin crania. 8 Department of Anthropology, University of Wisconsin-Madison, • We highlight morphological similarities between StW 578 and ‘Mrs Ples’. Madison, Wisconsin, USA 9 Department of Integrative Anatomical Sciences, Keck School of Medicine, University of Southern California, California, USA Introduction 10 South African Nuclear Energy The palaeocave infills of the Sterkfontein Caves, which lie 50 km northwest of Johannesburg (South Africa), are Corporation (Necsa), Pelindaba, well known for having yielded iconic fossil specimens, such as Sts 5 (‘Mrs Ples’) and StW 573 (‘Little Foot’).1 South Africa Fossiliferous deposits within the lower-lying Jacovec Cavern have provided additional hominin remains that are of 11 UCGT Department of Physics and Astronomy, Ghent University, Ghent, particular interest; prominent among them is the StW 578 cranium.2 StW 578 was discovered in 1995 partly in Belgium situ in ‘Orange’ sediments (Lo27 coordinates: Y, -73582.548; X, 2878771.407; Z, 1450.909) that are composed of partially calcified breccia exposed in the roof of the eastern part of the Jacovec Cavern2, and partly in collapsed CORRESPONDENCE TO: breccia beneath. Because of the conflicting geomorphological scenarios of the infilling of the lower chambers in Amélie Beaudet Sterkfontein2,3-7, determining a geological age for StW 578 is particularly challenging2,8-11. Absolute dating using cosmogenic nuclide burial methods originally provided an age of 4.02±0.27 Ma for the cranium.2 EMAIL: beaudet.amelie@gmail.com Together with the 3.67-million-year-old skeleton of StW 573, StW 578 represents some of the oldest evidence of human evolution in southern Africa.12 Because of its late Pliocene age, the StW 578 calotte (i.e. the top part of DATES: the cranium) is of great interest for reconstructing early hominin evolution. Late Pliocene fossiliferous deposits in Received: 14 July 2021 Revised: 06 Oct 2021 the Jacovec Cavern coincide with an important radiation of the genus Australopithecus, with the emergence of Accepted: 01 Oct. 2021 Australopithecus afarensis, Australopithecus deyiremeda, Australopithecus bahrelgahzali and the ‘Burtele Foot’.13 Published: 29 Mar. 2022 For instance, previous studies of the postcranial assemblage from the Jacovec Cavern revealed an interesting mosaic of features, with the femur having a very long neck relative to a small head but a round-sectioned shaft, HOW TO CITE: and with a clavicle (StW 606) that has morphological similarities to extant chimpanzees.2,14 Accordingly, StW 578 Beaudet A, Dumoncel J, Heaton JL, has the potential to contribute to our understanding of morphological variation and taxonomic diversity within Pickering TR, Clarke RJ, Carlson Australopithecus in the late Pliocene. KJ, et al. Shape analysis of the StW 578 calotte from Jacovec Cavern, Because the Jacovec cranium mainly preserves part of the calotte (Figure 1), along with fragments of the face Gauteng (South Africa). S Afr J Sci. 2022;118(3/4), Art. #11743. https:// and dentition, and a temporal bone (see Partridge et al.2; all initially cleaned and reconstructed by RJ Clarke), the doi.org/10.17159/sajs.2022/11743 taxonomic status of this specimen has been a matter of discussion. Indeed, in the original description, the authors refrained from attributing StW 578 to any species.2 Study of the cranial vault thickness and composition revealed ARTICLE INCLUDES: close affinities with the Australopithecus specimens from Sterkfontein Member 4.8 However, Partridge et al. noticed ☒ Peer review that: ☐ Supplementary material posterior to this fossa the tympanic plate slopes strongly posteriorly as it does in Pan, and DATA AVAILABILITY: in this respect differs from all other Australopithecus temporals from Sterkfontein Member ☐ Open data set 4, which resemble more closely the human, vertically inclined tympanic plate.2(p.609) ☐ All data included ☒ On request from author(s) The dental and facial morphology and the presence of a metopic ridge on the frontal convinced Clarke and Kuman12 ☐ Not available to classify this specimen as Australopithecus africanus rather than Australopithecus prometheus, teeth of which ☐ Not applicable also occur in the Jacovec sample. Research Article https://doi.org/10.17159/sajs.2022/11743 1 Volume 118| Number 3/4 March/April 2022 Shape analysis of StW 578 Page 2 of 6 EDITORS: Given the significance of this specimen and ongoing debates, we virtually reconstructed the StW 578 calotte Margaret Avery and compared its shape to those of extant humans, extant chimpanzees, and Australopithecus africanus (as Jemma Finch represented by Sts 5). Besides introducing a new protocol for the shape analysis of fossil hominin crania, we also provide new insights into the morphology of the Jacovec specimen. KEYWORDS: Australopithecus, Sterkfontein Caves, cranial morphology, surface-based comparison FUNDING: DSI-NRF, University of the Witwatersrand, AESOP+ program, Claude Leon Foundation, DSI- NRF Centre of Excellence in Palaeosciences, French Institute of South Africa, The Ghent University Special Research Fund (BOF. EXP.2017.0007), South African National Research Foundation (grant numbers 82591, 82611, 98808, 129336), PAST Figure 1: Virtual rendering of the StW 578 calotte in lateral right (top), superior (middle) and lateral left (bottom) views. Plaster used to physically reconstruct the cranium is in light grey and transparent. Material and methods Comparative material Our comparative sample of extant specimens comprised mixed-sex samples of non-pathological adult humans (Homo sapiens, n=6) and common chimpanzees (Pan troglodytes, n=6). Extant human samples were obtained from the Pretoria Bone Collection of the University of Pretoria15 while extant chimpanzee samples were obtained from the Royal Museum for Central Africa in Tervuren (Belgium). Additionally, we included the Australopithecus africanus specimen Sts 5 that comes from Sterkfontein Member 4, dated to about 2.8–2.4 Ma based on faunal assemblages.16-20 Sts 5 is currently housed in the Ditsong National Museum of Natural History (South Africa). Parts of the outer bone table of Sts 5 remained in the breccia during the initial preparation by Broom17,21, but this does not alter the overall shape of the cranial vault. Scanning and pre-processing step © 2022. The Author(s). Published StW 578 and Sts 5 were scanned at the microfocus X-ray tomography facility of the Palaeosciences Centre at the under a Creative Commons University of the Witwatersrand, in Johannesburg (South Africa), at a spatial resolution of 66.6 µm and 75.0 µm Attribution Licence. (isotropic voxel size), respectively. A 3D model of StW 578 is available on MorphoSource22. Extant humans and Research Article https://doi.org/10.17159/sajs.2022/11743 2 Volume 118| Number 3/4 March/April 2022 Shape analysis of StW 578 Page 3 of 6 chimpanzees have been similarly scanned at the South African Nuclear Shape analysis Energy Corporation in Pelindaba, South Africa, and at the Centre We compared StW 578 to extant specimens and Sts 5 by using landmark- for X-ray Tomography of Ghent University (UGCT) in Ghent, Belgium, free registration based on smooth and invertible surface deformation.26-30 with a resolution ranging from 70.0 µm to 102.3 µm. This approach has been previously applied to a number of craniodental and postcranial structures, including endocasts27,29, enamel-dentine As a pre-processing step, all of the crania were oriented the same way junctions28,31, vertebrae32 and bony labyrinths33 and comparisons with the opisthocranion and glabella aligned on a single transverse between the landmark-based and landmark-free approaches have plane, and a new image stack reflecting the standardised orientation revealed the ability of the latter approach for capturing geometric details was generated using Avizo v9.023 (FEI Visualization Sciences and for statistical determination of geometric correspondence34. Because Group Inc., https://www.fei.com/software/amira-avizo/)8. The same the StW 578 calotte is partial, instead of using the whole surface to transverse plane was used to virtually cut the crania so that the superior align specimens as in previous studies27-29, we used four landmarks, part of the braincase (that is preserved in StW 578) could be i.e. glabella, opisthocranion, and two landmarks positioned on the separated from the rest of the cranium and studied. Finally, because external surfaces of the right and left parietal bones at the we were interested in the external shape of the cranium only, we intersection of (1) a coronal plane positioned at three-quarters of the virtually isolated the external surface from the inner surface. maximum length of the calotte and of (2) the transverse plane that was used for isolating the top of the calotte. Surfaces were aligned in position, orientation and scale using one surface that was randomly Reconstruction of StW 578 selected as a reference and by using the tool ‘Landmark Surface Before virtually reconstructing the StW 578 calotte, we removed the Warp’ (method: Rigid + Uniform Scale) in Avizo v9.0 which is based plaster using segmentation tools in Avizo v9.0 (STEP1, Figure 2A). on the iterative closest point algorithm that minimises the root mean We fitted a surface through StW 578 using the tool ‘Patch’ in square distance between the points of each specimen to Rhinoceros 3D v6.024 (STEP2, Figure 2B). The resulting surface corresponding points on the reference.35 A template was deformed to (Figure 2B) was opened in Avizo v9.0 and the parts of the new surface extant specimens using Deformetrica v4.26,36,37 The extant specimens that filled in the gaps between bones were manually extracted (Figure and Sts 5 were deformed to StW 578. Based on this computation, the 2C) and merged with the initial surface using the tool ‘Flatten visible parts of the frontal and parietal bones that are missing in StW 578 (Figure layer’ in Meshlab25 (STEP3, Figures 2D,E). This new surface was 2E) were systematically removed from the comparative extant and mirrored to reconstruct missing regions in the opposite side (Figure fossil specimens using an automated method.29,30,36 We then deformed 2F). Finally, STEP2 and STEP3 were repeated (Figure 2G,H). Inferior another template to the extant comparative surfaces generated after this portions of the parietal and frontal bones were still missing at this stage step and a global mean shape as well as taxon-specific mean shapes (Figure 2E). Because these regions cannot be reconstructed using (Homo sapiens and Pan troglodytes, each n=6) were generated. Finally, existing bones, we preferred not to estimate them and thus the global mean shape and taxon mean shapes were deformed to StW systematically removed the homologous regions in all comparative 578 and Sts 5. The resulting 3D deformation fields that integrate local specimens (see below). orientation and the amplitude of the deformation were analysed using principal component analysis (PCA) (Figure 3). Displacements Similarly, we removed the plaster in Sts 5 and the missing regions were from the taxon mean shapes to StW 578 and from Sts 5 to StW 578 virtually filled in by applying STEP2 and STEP3. were rendered by colour maps. Figure 2: Successive steps for the virtual reconstruction of the StW 578 cranium. The initial surface (A) has been wrapped using a patch (B) and the gaps reconstructed (C) and merged with the initial surface (D). To the end result of the first iteration (E), a mirror was applied (F) and the overall process repeated (G). The resulting surface is lacking lateral portions of the frontal and parietal bones (H) indicated by a star. Research Article https://doi.org/10.17159/sajs.2022/11743 3 Volume 118| Number 3/4 March/April 2022 Shape analysis of StW 578 Page 4 of 6 in extant humans (in which the rounded forehead contributes to the globular aspect of the overall cranium) as emphasised by the large pink to red area in the colour maps. Compared with the extant chimpanzees, the parietal and frontal bones of the StW 578 calotte are significantly more elevated, which is shown in Figure 3C by the cranial vault being nearly entirely red. The shapes of the external surfaces of the tops of the calottes of StW 578 and Sts 5 are closely similar (Figure 3D), with only minimal differences in the superior part of the frontal bone and the lateral surface of the parietal bones. Finally, we investigated how our virtual reconstruction of StW 578 may influence our shape analysis by applying the same protocol to the bones preserved in the original specimen and comparing the morphology to the extant groups. If we consider the results of the deformation-based shape comparison of the regions of the calotte that are preserved in StW 578 and artificially isolated in the extant comparative sample (Figure 4), StW 578 plots closer to the extant human cluster along PC1 that represents 93.2% of the variation. Here again, StW 578, extant humans and extant chimpanzees overlap along PC2 that represents 2.0% of the variation. We thus obtain similar results as in the first set of deformation that includes our reconstruction of the calotte, which tends to suggest that our reconstruction does not bias the result of the shape analysis. Figure 3: Principal component (PC) analysis of the deformation-based shape comparisons of the StW 578 and Sts 5 calottes and of the extant human and chimpanzee calottes (A). Comparative maps of morphological deformations from the taxon-specific mean shapes computed for extant humans (B) and extant chimpanzees (C) to StW 578 and from Sts 5 to StW 578 (D) Figure 4: Principal component (PC) analysis of the deformation-based in superior view. The colour bar represents the number of shape comparisons of the unreconstructed upper part of the deformations. StW 578 calotte and of the extant human and chimpanzee To estimate potential bias induced by our reconstruction of StW calottes, focusing on bones originally preserved in StW 578 578 (Figure 2) in the shape analysis, we computed a second set of and artificially isolated in the comparative sample. deformations using the original surface of the StW 578 calotte (i.e. not reconstructed, neither physically nor virtually). The regions that Discussion correspond to the missing bone in StW 578 were automatically removed from the extant specimens by using the results of the first set of Because of its fragmentary nature, the taxonomic and phylogenetic deformations.29,36 We then computed a PCA using the deformation fields status of the StW 578 calotte remains debatable, although it has been generated by this second set of deformation (Figure 4). recently assigned to A. africanus by Clarke and Kuman12. Within the limits of our sample, our comparative shape analysis reveals morphological Results differences with the cranial vault of extant humans, mainly located in the frontal bones and on the lateral surface of the parietal bones, and more Figure 3A shows the PCA of the deformation-based shape comparison dramatically with the cranial vault of extant chimpanzees. As such, our of StW 578 and extant and fossil comparative specimens. The two extant study further clarifies the polarity (i.e. derived or ancestral) of the cranial comparative groups are well discriminated along PC1, which accounts features identified in StW 578.2 for 95.0% of the variation. Chimpanzees plot in positive space while extant humans plot in negative space. Along PC1, both StW 578 and The hominin cranium is highly integrated.38 Frontal bone morphology Sts 5 plot close to each other and closer to the extant human cluster in reflects the integration of the bone structures of the upper face and negative space. Along PC2, which represents 1.8% of the variation, the anterior neurocranium.39 Within this context, the marked differences two comparative groups and the fossil specimens mostly overlap. identified in the frontal bones of StW 578 and extant humans by our comparative shape analysis might reflect the primitive morphology The nature and extent of the differences between StW 578 and the of the upper face in Australopithecus. Indeed, the hominin face has comparative specimens were investigated using topological mapping of experienced dramatic changes through time, with the earliest changes interspecific variation (Figure 3B–D). Compared with extant humans, the affecting primarily the canines and supraorbital regions (potentially lateral part of the parietal bones in StW 578 is slightly more elevated as associated to social interactions) and later modifications related to the indicated by the white spots on both sides of the cranial vault in Figure 3B. masticatory apparatus and a transition from tough and hard to soft or pre- On the contrary, the frontal bones in StW 578 are more flattened than processed food.40 On the other hand, within the frame of the hypothesis Research Article https://doi.org/10.17159/sajs.2022/11743 4 Volume 118| Number 3/4 March/April 2022 Shape analysis of StW 578 Page 5 of 6 of modularity of the hominin face and neurocranium, we might consider Competing interests the possibility that differences in the frontal bone could be the result We have no competing interests to declare. of neutral evolution.41,42 Alternatively, this result might be explained by the influence of the frontal and temporal lobes on the morphology of the frontal bones.43 However, because significant reorganisation of the Authors’ contributions frontal and temporal lobes occurred in later hominins44,45, this hypothesis Conceptualisation: A.B.; methodology: A.B., J.D.; data collection – is unlikely. Lastly, it is noteworthy that the extant human frontal bones excavations: R.J.C., D.S., J.L.H., T.R.P.; data collection – scanning: are characterised by the presence of two bosses which are absent in L.V.H., L.B.; K.J.C.; data analysis: A.B., K.C.; writing – the initial draft: fossil hominins.46 Nonetheless, these results are preliminary and will A.B.; writing – revisions: A.B., D.S., R.J.C., K.J.C., J.D., L.V.H., L.B., need to be further supported by future analyses including a large extant J.L.H., T.R.P.; funding acquisition: A.B., D.S. human sample. The assessment of the cranial vault thickness variation in StW 578 References demonstrated particularly thick parietal bones, which differs from 1. Stratford DJ. A review of the geomorphological context and stratigraphy of the pattern of cranial thickness reported for extant humans and the Sterkfontein Caves, South Africa. In: Klimchouk A, Palmer AN, De Waele extant chimpanzees (see Fig. 8 in Beaudet et al.8). 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J Hum Evol. fact that the present preliminary results derive from a new protocol, our 2010;59(1):70–86. https://doi.org/10.1016/j.jhevol.2010.03.014 results should be carefully considered and future analyses should help clarify this question. 8. Beaudet A, Carlson KJ, Clarke RJ, De Beer F, Dhaene J, Heaton J, et al. Cranial vault thickness variation and inner structural organization in the Acknowledgements StW 578 hominin cranium from Jacovec Cavern, South Africa. J Hum Evol. 2018;121:204–220. https://doi.org/10.1016/j.jhevol.2018.04.004 We are indebted to E. Gillisen and W. Wendelen (Tervuren), G. Krüger and E. L’Abbé (Pretoria), L. Kgasi, H. Fourie and S. Potze (Pretoria), and 9. Bruxelles L, Clarke RJ, Maire R, Ortega R, Stratford D. Stratigraphic analysis S. Jirah and B. Zipfel (Johannesburg) for granting us access to fossil of the Sterkfontein StW 573 Australopithecus skeleton and implications and comparative material in their care. We also thank J. Hoffman and F. for its age. J Hum Evol. 2014;70:36–48. https://doi.org/10.1016/j. de Beer (Pelindaba), and M. Dierick (Ghent) for X-ray microtomographic jhevol.2014.02.014 acquisitions. We are grateful to the Ditsong National Museum of Natural 10. Bruxelles L, Stratford DJ, Maire R, Pickering TR, Heaton JL, Beaudet A, et al. A History and the University of the Witwatersrand for loaning hominin multiscale stratigraphic investigation of the context of StW 573 ‘Little foot’ and crania in their collections. For technical and/or scientific discussion/ Member 2, Sterkfontein caves, South Africa. J Hum Evol. 2019;133:78‑98. collaboration we are grateful to: M. Carmen Arriaza (Johannesburg), https://doi.org/10.1016/j.jhevol.2019.05.008 G. Krüger (Pretoria), K. Kuman (Johannesburg), E. L’Abbé (Pretoria), A. Oettlé (Pretoria) and J.F. Thackeray (Johannesburg). We thank the Editor 11. Stratford DJ, Grab S, Pickering TR. The stratigraphy and formation history of and two anonymous reviewers for their comments. 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