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A 3.8-million-year-old hominin cranium from Woranso-Mille, Ethiopia

Nature volume 573, pages 214–219 (2019)Cite this article

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Abstract

The cranial morphology of the earliest known hominins in the genus Australopithecus remains unclear. The oldest species in this genus (Australopithecus anamensis, specimens of which have been dated to 4.2–3.9 million years ago) is known primarily from jaws and teeth, whereas younger species (dated to 3.5–2.0 million years ago) are typically represented by multiple skulls. Here we describe a nearly complete hominin cranium from Woranso-Mille (Ethiopia) that we date to 3.8 million years ago. We assign this cranium to A. anamensis on the basis of the taxonomically and phylogenetically informative morphology of the canine, maxilla and temporal bone. This specimen thus provides the first glimpse of the entire craniofacial morphology of the earliest known members of the genus Australopithecus. We further demonstrate that A. anamensis and Australopithecus afarensis differ more than previously recognized and that these two species overlapped for at least 100,000 years—contradicting the widely accepted hypothesis of anagenesis.

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Fig. 1: The MRD-VP-1/1 cranium.
Fig. 2: Comparisons of upper canine morphology.
Fig. 3: Structure of the face and neurocranium.

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Data availability

The data that support the findings of this study that were not included in the Supplementary Information are available from the corresponding authors upon reasonable request.

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Acknowledgements

We thank the Authority for Research and Conservation of Cultural Heritage (ARCCH) for permission to conduct field and laboratory work; the Afar people of Woranso-Mille and the Mille District administration for their hospitality; the project’s fieldwork crew members for their tireless support of field activities; The National Museum of Kenya, National Museum of Tanzania, Ditsong Museum and the Evolutionary Studies Institute of South Africa for access to original hominin specimens in their care; Max Planck Institute for Evolutionary Anthropology for access to comparative hominin computed tomography scan data; T. White, G. Suwa and B. Asfaw for access to the original A. ramidus material and for providing images and unpublished measurements; M. Brunet and F. Guy for images and unpublished measurements of S. tchadensis; W. H. Kimbel for informative discussions and for access to a surface model of the A.L. 444-2 cranium; D. Lieberman (the Peabody Museum (Harvard)), R. Beutel (Phyletisches Museum Jena), C. Funk (Museum für Naturkunde), M. Tocheri (National Museum of Natural History (Smithsonian)), U. Olbrich-Schwarz (the Max Planck Institute for Evolutionary Anthropology) for the use of computed tomography scans of extant apes; A. Girmaye, M. Endalamaw, Y. Assefa, T. Getachew, S. Melaku and G. Tekle of ARCCH for access to the fossil collections housed in the Paleoanthropology Laboratory in Addis Ababa; T. Stecko from the Penn State Center for Quantitative Imaging for assistance with computed tomography scanning; and N. Meisel and D. N. Kaweesa (Made By Design Lab (Pennsylvania State University)) for assistance in 3D printing. This research was supported by grants from the US National Science Foundation (BCS-1124705, BCS-1124713, BCS-1124716, BCS-1125157 and BCS-1125345) and The Cleveland Museum of Natural History. Y.H.-S. was also supported by W. J. and L. Hlavin, T. and K. Leiden, and E. Lincoln. S.B. was supported by the European Research Council (ERC) under the European Union’s Horizon 2020 research and innovation programme (ERC-724046-SUCCESS; http://www.erc-success.eu). S.M.M. was supported by the Max Planck Institute for Evolutionary Anthropology, Department of Human Evolution.

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Author notes

  1. These authors contributed equally: Yohannes Haile-Selassie, Stephanie M. Melillo

Authors and Affiliations

  1. Department of Physical Anthropology, Cleveland Museum of Natural History, Cleveland, OH, USA

    Yohannes Haile-Selassie

  2. Department of Human Evolution, Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany

    Stephanie M. Melillo

  3. Department of Cultural Heritage, University of Bologna, Ravenna, Italy

    Antonino Vazzana & Stefano Benazzi

  4. Department of Anthropology, Pennsylvania State University, University Park, PA, USA

    Timothy M. Ryan

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Contributions

Y.H.-S. and S.M.M. conducted fieldwork and collected data. T.M.R. scanned the specimen using computed tomography. T.M.R., S.B. and A.V. performed the three-dimensional reconstruction with contributions from Y.H.-S. and S.M.M. Y.H.-S. and S.M.M. performed the comparative analysis. S.M.M. and Y.H.-S. wrote the paper with contributions from T.M.R., S.B. and A.V.

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Correspondence to Yohannes Haile-Selassie or Stephanie M. Melillo.

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Peer review information Nature thanks Craig S. Feibel, John W. Kappelman and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

Extended data figures and tables

Extended Data Fig. 1 MRD-VP-1/1 digital reconstructions.

Digitally reconstructed cranium and comparison of three alternative reconstructions. a–f, The reconstructed cranium MRD- Sts 5 is shown in anterior view (a), posterior view (b), superior view (c), left (d) and right (e) lateral views and inferior view (f). Additional images illustrate minor differences in reconstructed zygomatic arches. g, MRD-Sts 5. h, MRD-A.L. 444-2. i, MRD-WT 17000. j, MRD-Sts 5 with edges superimposed to the three different restored versions: MRD-Sts 5 (blue lines); MRD-A.L. 444-2 (green lines) and MRD-WT 17000 (red lines). Scale bars, 2 cm.

Extended Data Fig. 2 Basic steps involved in repositioning and reconstructing the MRD face.

a, Midsagittal planes computed for the original neurocranium (ivory) and facial portion (red). b, The original facial portion is rotated to align the midsagittal plane of the face with the midsagittal plane of the neurocranium, then the former is moved along the midsagittal plane to establish contact with the latter. c, The left supra-orbital bone was mirrored and aligned to the original MRD right side. d, The complete right side was mirrored and aligned to the left side. e, f, Anterior (e) and inferior (f) views of the original left maxillary dental arcade and part of the palate superimposed to the mirrored copy of the right hemiface. g, h, Frontal (g) and basal (h) view of the right dental arcade reconstructed by mirroring the left dental arcade (except for the right M3). Mirrored portions are shown in green. Scale bar, 4 cm. See Methods for details.

Extended Data Fig. 3 MRD symmetrization using a reflected relabelling procedure and neurocranium reconstruction.

a, The template with landmarks (red), non-osteometric homologous landmarks (blue), curve semilandmarks (light blue) and surface semilandmarks (yellow) was digitized on the MRD cranium. b, The template configuration with names of landmarks and curves numbers (Supplementary Note 2). c, Basal view of the template digitized on the MRD cranium. d, The template digitized on the mirrored cranium. e, Symmetric configuration of the (semi)landmarks and warped surface. f, Basal view of the final result for MRD-sym. g, Basal view of the left zygomatic process, the right mastoid process and other parts of the basicranium reconstructed by mirroring the original counterparts (integrated parts are shown in green). h, Basal view, final result after integrating the mirrored counterparts. Scale bars, 2 cm. See Methods for details.

Extended Data Fig. 4 Integration of missing parts using Sts 5.

a, Template built on the cranium of A. africanus (Sts 5). Templates with landmarks (red), curve semilandmarks (light blue) and surface semilandmarks (yellow) were digitized on Sts 5. b, Template configuration with names of landmarks and curves numbers (labels are related to Supplementary Note 3). c, The same set of (semi)landmarks on the MRD-sym cranium. d, TPS interpolation of the Sts 5 cranium, warped to MRD-sym (blue and grey, respectively). e–h, MRD-sym with the integrated missing parts (blue) isolated from the resulting warped surfaces obtained by the deformation of Sts 5 (shown here as an example) in anterior (e), left lateral (f), inferior (g) and superior (h) views. Scale bar, 4 cm.

Extended Data Fig. 5 Integration of missing parts using A.L. 444-2 and KNM-WT 17000.

a, e, Templates with landmarks (red), curve semilandmarks (light blue) and surface semilandmarks (yellow) digitized on A.L. 444-2 (a) and KNM-WT 17000 (e) crania. b, f, The configurations of (semi)landmarks with names of landmarks and curves numbers digitized on A.L. 444-2 (b) and KNM-WT 17000 (f) crania (labels are related to Supplementary Notes 4, 5). c, g, Sets of (semi)landmarks on the MRD-sym cranium. d, h, TPS interpolation of the A.L. 444-2 (green) and KMN-WT 17000 (red) crania warped to MRD-sym (grey). Scale bar, 4 cm.

Extended Data Fig. 6 Canine orientation in MRD and KNM-KP 29283.

The method for measuring the implantation angle of the upper canine is shown in a, b. a, The internal alveolar plane was established by best-fitting a plane (outlined in blue) to three landmarks between left P3 and P4, between right P3 and P4 and between left M1 and M2. b, Landmarks were placed at the root tip and at the occlusal-most incursion along the distal enamel line. Upper canine implantation was measured in lateral view as the two-dimensional angle (θ) between a line connecting the canine landmarks and the axis of the alveolar plane. c, d, Upper canine implantation in the fossil specimens. c, A. anamensis paratype maxilla KNM-KP 29283. d, MRD. Of the other two A. anamensis maxillae currently known, one (KNM-KP 58579) is qualitatively similar to KNM-KP 29283 and the other (ARA-VP-14/1) is more inclined. Scale bar, 1 cm. The scale bar applies to images in c and d. e, The magnitude of difference in canine implantation angle between MRD and KNM-KP 29283 (12.5°, red dashed line) is shown in the context of expected conspecific differences. The expectation distributions were constructed using a permutation approach, for which the measurements from two individuals were randomly drawn (without replacement) from a comparative sample and the difference in orientation angle was computed. This procedure was repeated 500 times, separately for comparative species P. troglodytes and G. gorilla (Supplementary Note 6.2).

Extended Data Fig. 7 Maxillary arcade shape.

Maxillae in occlusal view of select A. afarensis and A. anamensis specimens and MRD (original, as preserved). The canine and postcanine teeth form a nearly straight line in A. anamensis and MRD. By contrast, the canine tends to be slightly medially offset relative to the postcanine row in many A. afarensis specimens. The position of the canine is indicated by the black asterisk. Scale bar, 1 cm.

Extended Data Fig. 8 Comparison of crania in lateral view.

Red lines and arrows show the inclination of the frontal and the presence of a post-toral sulcus, respectively. Blue lines show the orientation of the mid and lower face, with an broken line indicating a segmented facial profile27. The green arrow marks the anterior projection of the zygomatic tubercle (relative to the anterior zygomatic root). Scale bar, 2 cm.

Extended Data Fig. 9 Comparison of crania in posterior view.

The transverse contour of the cranial base is convex in African apes, whereas A. afarensis shows an angular transition between the nuchal region and the greatly expanded mastoids (red dashed lines). In this regard, A. afarensis anticipates the morphology of robust australopiths, but A. africanus is less derived. MRD shows the primitive convex contour of the base, even though the mastoids are expanded. MRD is also primitive with regard to the great length of the nuchal plane (black arrows). However, it is similar to A. afarensis in the configuration of the compound temporal–nuchal crest (white dashed lines), the bare area (blue hatched triangle), and the overall ‘bell-shaped’ posterior outline (that is, the parietal walls are slightly convergent superiorly and the greatest width occurs basally across the enlarged mastoids).

Extended Data Fig. 10 Results of phylogenetic analyses.

a, Cladogram resulting from the character matrix of ref. 27, with the addition of MRD and previously described A. anamensis specimens (combined as a single OTU, K-combined). Parsimony analysis returned a single most-parsimonious tree (l = 196, C = 0.71, R = 0.70). b, Cladogram resulting from the character matrix of ref. 33 (and references therein) with the addition of the combined MRD–A. anamensis OTU (S&G-combined). This analysis returned a single most-parsimonious tree (l = 429, C = 0.47, R = 0.66) with identical topology. The position of the combined MRD–A. anamensis OTU reinforces accepted relationships and is consistent with geochronology. c–g, Cladograms resulting from analyses in which MRD is treated as a separate OTU (that is, an OTU bearing observations primarily for cranial characters, but very few dental characters and no mandibular characters.) c, d, Equally parsimonious cladograms from the K-separate analysis (l = 196, C = 0.71, R = 0.68). e–g, Equally parsimonious cladograms from the S&G-separate analysis (l = 430, C = 0.47, R = 0.66). The ‘pre-2004 A. anamensis’ OTU in e–g bears observations primarily on dentognathic characters. Character scores for MRD are provided in Supplementary Table  1, sheets 1 and 2. Regardless of whether cranial or dentognathic characters are considered, the phylogenetic placement of MRD and the previously known A. anamensis sample remains stable relative to other hominins. h, i, Cladograms from the K-combined and S&G-combined analyses (as in a and b), with apomorphies added to the cladograms to illustrate the implied pattern of evolutionary change. The character states reconstructed at nodes A and B provide the reference for identifying A. anamensis and A. afarensis apomorphies, which are shown here as rectangles containing their abbreviated character labels. Characters in red, orange, gold and green describe similar morphology and appear in both previously published studies27,33. See Supplementary Note 9 and Supplementary Table  1.

Supplementary information

Supplementary Information

This file contains Supplementary Notes 1-10 and Supplementary Tables S6.1, S9.1, S9.2 and S9.3.

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Supplementary Table

This file contains Supplementary Table 1: MRD character scores.

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Haile-Selassie, Y., Melillo, S.M., Vazzana, A. et al. A 3.8-million-year-old hominin cranium from Woranso-Mille, Ethiopia. Nature 573, 214–219 (2019). https://doi.org/10.1038/s41586-019-1513-8

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