Materials

As comparative materials, we included a cast of the specimen AL 333-83 from the Hadar Formation recovered during the field seasons of 1974–197727 and that is currently housed at the Cleveland Museum of Natural History. AL 333-83 represents a partial atlas that preserves most of the left side, including the inferior and superior articular facets and a portion of the posterior arch, but it is missing the left transverse process27 (Fig. 2). Additionally, for measuring dimensions of the carotid canal, we investigated 10 southern African fossil hominin crania from the sites of Makapansgat (Member 4), Sterkfontein (Member 4) and Swartkrans (Member 1) (Supplementary Tables S1, S2; for further details see Beaudet et al.40,47,57).

Our comparative sample of extant specimens comprised 30 atlases of non-pathological adult Homo, Pan, Gorilla and Pongo sampling males and females, and 15 basicrania (humans and common chimpanzees only) (Supplementary Tables S1, S2).

Virtual reconstruction of the atlas

The skull of StW 573 and the StW 679 atlas were scanned at the microfocus X-ray tomography facility of the Palaeosciences Centre at the University of the Witwatersrand, in Johannesburg (South Africa), at a spatial resolution of 88 µm and 19 µm, respectively (isotropic voxel size). All comparative specimens investigated in this study were imaged by X-ray tomography using various systems58,59 (Supplementary Tables S1, S2). Most of the comparative extant specimens have been downloaded from MorphoSource (https://www.morphosource.org/) and from the Digital Morphology Museum KUPRI (http://dmm.pri.kyoto-u.ac.jp/dmm/WebGallery/dicom/researcherTop.html; Supplementary Tables S1, S2). The cast of AL 333-83 has been rendered by using photogrammetry. Four of the extant human specimens have been imaged by using a Next Engine scanner.

The atlas of StW 573 was virtually extracted from the skull using Avizo v9.0 (Visualization Sciences Group Inc.) combining the watershed tool and manual corrections60,61. We reconstructed the missing portions of the left transverse process by mirroring the intact right transverse process (Fig. 2).

Surface-based comparisons

We investigated morphology of the atlas by using a size-independent and landmark-free registration method based on smooth and invertible surface deformation36,62. As a pre-processing step, surfaces were automatically aligned in position, orientation and scale with respect to one surface randomly selected using the Iterative Closest Point (ICP) algorithm63. From this set of pre-aligned surfaces, an automatic non-rigid registration process was performed on the extant specimens only (i.e., Homo, Pan, Gorilla, and Pongo) via the deformation of a template using the software Deformetrica36,62 (available online at http://www.deformetrica.org/). A global mean shape and the deformation fields from the global mean shape to each extant specimen were computed from the set of aligned surfaces. Then, the global mean shape was subsequently deformed to StW 573, StW 679 and AL 333-83. Moreover, taxon mean shapes were generated for each extant group and deformed to StW 573.

Because StW 679 and AL 333-83 are incomplete, we performed a second analysis focusing on the left articular facets following the protocol published in Dumoncel et al.35 and Beaudet et al.36. Non-common regions of the atlases (i.e., regions not preserved in StW 679 and AL 333-83) were automatically eliminated from the sample so that all of the specimens contain only comparable information that can be used for the new registration process. This step has been automatically performed by using the deformation of the global mean shape to the extant and fossil specimens of the first analysis (see Fig. 1 in Beaudet et al.36). Subsequently, partial atlases were re-aligned using the ICP algorithm and the same reference as we used for the first analysis. In this manner, we computed a second analysis, including a second global mean shape and corresponding taxon mean shapes, from the set of partial atlases of using extant specimens only. The global mean shape and the taxon mean shapes were subsequently deformed to the partial atlases of StW 573, StW 679 and AL 333-83, providing deformation fields from the global mean shape to each fossil specimen.

Deformation fields integrating local orientation and the amplitude of deformations from the global mean shape to each specimen were statistically analysed by a principal component analysis (PCA) using the package ade4 for R64 (Fig. 3). The fossil specimens were subsequently projected into shape space. Thus, we computed two separate PCAs, i.e., a first one with the complete atlases (excluding StW 679 and AL 333-83, Fig. 3a) and a second one with the partial atlases (including the two partial fossil specimens and StW 573, Fig. 3b). Cumulative displacement variations are rendered and visualized using a pseudo-colour scale ranging from dark blue (lowest values) to red (highest values; Fig. 3). In addition to colour maps, we used vectors representing local maxima of the displacements. We computed a backtransform morphospace, i.e., representative shapes computed from the deformation fields are superimposed to the PCA to show how shape varies across the morphospace (see Olsen65 for an example based on 2D landmarks; Fig. 3). Colour scale represents variation from the global mean shape computed for the entire extant sample.

Linear measurements

We used standard measurements reported in Gómez-Olivencia et al.44 and illustrated in Figure S2A for measuring dimensions of the atlas of StW 573 and those in the comparative extant sample. Because StW 679 and AL 333-83 are incomplete and could not be virtually reconstructed due to the absence of the anterior and posterior vertebral arches, we could not estimate on them any of the metric variables used in this study, except for the size of the left superior articular facet in StW 679. We used the product of the diameter in the major axis (1L/R) and the orthogonal diameter (2L/R) of each facet as an estimation of the area of the articular surface. Moreover, we divided the diameter in the major axis by the orthogonal diameter to assess a ratio between the length and breadth of each facet.

Cross-sectional areas of the vertebral foramen and transverse foramina

We measured cross-sectional areas of the vertebral foramen (VFA) and the right (RFA) and left (LFA) transverse foramina (Supplementary Fig. S2B). In order to do this, we first defined the best-fit plane to the atlas using the module ‘Points to Fit’ in Avizo v9.0. This plane was moved to pass between superior and inferior articular facets when measuring the VFA, and through the most lateral points of the right and left transverse processes when measuring the RFA and LFA. A 2D section was extracted for both positions. Cross-sectional areas of the vertebral foramen and of the foramina were measured on the respective 2D sections by segmenting the canal and foramina using the module ‘Material statistics’ in Avizo v9.0. For standardizing measurements, we divided areas by the product of the length (i.e., from the most lateral tip of the right transverse process to the most lateral tip of the left transverse process) and width of the atlas (i.e., the most anterior point of the anterior arch to the most posterior point of the posterior arch). Only RFA could be measured in StW 679, while AL 333-83 preserves neither transverse process (Fig. 2).

Cross-sectional area of the carotid canal

To avoid any potential distortions related to the presence of bony eminences surrounding the external opening or to torsion of the canal, we measured cross-sectional areas (CSA) of the left carotid canal at mid-distance between the external opening of the canal and the bending of the canal observed when entering the petrous bone (Supplementary Fig. S3). First, we placed landmarks on the aperture and defined a best-fit plane using the module ‘Points to Fit’ in Avizo v9.0 (Supplementary Fig. S3). This position was considered to represent the external opening of the canal (plane C in Supplementary Fig. S3). This plane was moved until reaching the ‘elbow’ of the canal in the petrous bone, after which the position was noted as representing the ‘elbow’ of the canal (plane A in Supplementary Fig. S3). Subsequently, the plane was moved and positioned equidistant between the two previously identified positions (i.e., the opening and the ‘elbow’) before virtually extracting the corresponding 2D plane and subjecting it to further measurements (plane B in Supplementary Fig. S3). Cross-sectional area of the carotid canal was measured by segmenting the canal and using the module ‘Material statistics’ in Avizo v9.0. As the portion of the carotid canal between the opening and the ‘elbow’ is partially filled with sediments in SK 847, we extracted a plane parallel to the plane passing through the foramen and that samples the best-preserved part of the bony canal. Accordingly, this measurement could not be directly compared to the rest of the sample, but it could be used as an approximation of the early Homo condition.

Estimation of brain glucose utilization

We estimated brain glucose utilization (BGU) in StW 573 by using the equation provided by Boyer and Harrington24, i.e., ln(BGU) = 1.17*ln(ACA)−0.10, where ACA represents twice the sum of the respective averages of transverse foramen cross-sectional area and carotid canal cross-sectional area. Since the endocast of StW 573 is distorted36, we could not include the cranial capacity in the equation as recommended by the authors24. For extant comparative specimens, we used the mean, minimum and maximum values of CSA, RFA and LFA for computing the mean, minimum and maximum values of ACA (Table 4 and Supplementary Table S3). For fossil comparative specimens, we used cross-sectional area of the transverse foramen preserved in StW 679 as a proxy estimate for Australopithecus specimens. Because of the degree of variation in the measurement of the cross-sectional area of the transverse foramina of extant samples (e.g., up to 7% of differences between the right and left transverse foramina in Homo, Table 2), and because we could not account for inter-individual variation in transverse foramina in the Australopithecus sample, our computations of the ACA in the comparative Australopithecus specimens should be considered as initial provisional estimations. However, we tentatively estimated ranges of variations for fossil specimens by using the standard deviation of RFA and LFA of extant humans and extant chimpanzees and recomputing values for ACA and BGU (Table 4).