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The position of Australopithecus sediba within fossil hominin hand use diversity

Nature Ecology & Evolution volume 4, pages 911–918 (2020)Cite this article

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Abstract

The human lineage is marked by a transition in hand use, from locomotion towards increasingly dexterous manipulation, concomitant with bipedalism. The forceful precision grips used by modern humans probably evolved in the context of tool manufacture and use, but when and how many times hominin hands became principally manipulative remains unresolved. We analyse metacarpal trabecular and cortical bone, which provide insight into behaviour during an individual’s life, to demonstrate previously unrecognized diversity in hominin hand use. The metacarpals of the palm in Australopithecus sediba have trabecular morphology most like orangutans and consistent with locomotor power-grasping with the fingers, while that of the thumb is consistent with human-like manipulation. This internal morphology is the first record of behaviour consistent with a hominin that used its hand for both arboreal locomotion and human-like manipulation. This hand use is distinct from other fossil hominins in this study, including A. afarensis and A. africanus.

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Fig. 1: Average relative trabecular bone (RBV) distribution in great ape and human metacarpals during habitual hand postures.
Fig. 2: Relative trabecular bone volume fraction (RBV) distribution in the metacarpal heads of the palm.
Fig. 3: Relative trabecular bone volume fraction (RBV) distribution in the thumb metacarpal.
Fig. 4: Relative cortical bending stiffness of thumb metacarpals at midshaft.

Data availability

The data used to generate the analyses and graphs are available at: https://data.kent.ac.uk/id/eprint/111

Code availability

All computational functions in the Methods are available in the software described in Supplementary Table 7.

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Acknowledgements

We thank I. Livne (Powell-Cotton Museum), A. vanHeteren and M. Hiermeier (Zoologische Staatssammlung München), C. Boesch and U. Schwarz (Max Planck Institute for Evolutionary Anthropology), A. Ragni (Smithsonian Institution, National Museum of Natural History); M. Teschler-Nicola and R. Muehl (Natural History Museum, Vienna), J. Moggi-Cecchi and S. Bortoluzzi (University of Florence), F. Mayer (Museum für Naturkunde—Leibniz Institute for Evolution and Biodiversity Science, Berlin), B. Großkopf (Johann-Friedrich-Blumenbach-Institut für Zoologie und Anthropologie der Georg-August-Universität Göttingen), R. Macchiarelli (Museo Nazionale Preistorico Etnografico ‘Luigi Pigorini’), B. Zipfel (University of the Witwatersrand), E. Gilissen and W. Wendelen (Musée Royal de l’Afrique Centrale), V. Volpato (Senckenberg Museum of Frankfurt), D. Nadel (University of Haifa) and I. Herskovitz (Tel Aviv University) for access to specimens in their care. We also thank D. Plotzki (Max Planck Institute for Evolutionary Anthropology) and K. Smithson (Cambridge Biotomography Centre) for assistance in scanning these specimens, as well as M. Tocheri for assistance with landmarking software and L. Georgiou for discussions that enhanced this manuscript. For the Malapa project, we thank the South African Heritage Resources Agency and the Nash family for permissions, and the South African National Centre of Excellence in PalaeoSciences, the Lyda Hill Foundation, South African Department of Science and Technology, the South African National Research Foundation, the Evolutionary Studies Institute, University of the Witwatersrand, the University of the Witwatersrand’s Vice Chancellor’s Discretionary Fund, the National Geographic Society, the Palaeontological Scientific Trust, the Andrew W. Mellon Foundation, the Ford Foundation, the U.S. Diplomatic Mission to South Africa, the French embassy of South Africa, the Oppenheimer and Ackerman families, and Sir Richard Branson for funding. This research was supported by the Spanish MICINN/FEDER (CGL2016-75109-P), European Research Council starting grant no. 336301, European Union’s Horizon 2020 research and innovation programme (grant no. 819960), the Max Planck Society and the Fyssen Foundation.

Author information

Authors and Affiliations

  1. Skeletal Biology Research Centre, School of Anthropology and Conservation, University of Kent, Canterbury, UK

    Christopher J. Dunmore, Matthew M. Skinner, Ameline Bardo & Tracy L. Kivell

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

    Matthew M. Skinner, Jean-Jacques Hublin & Tracy L. Kivell

  3. Evolutionary Studies Institute, University of the Witwatersrand, Johannesburg, South Africa

    Matthew M. Skinner, Lee R. Berger & Tracy L. Kivell

  4. Chaire Internationale de Paléoanthropologie, Collège de France, Paris, France

    Jean-Jacques Hublin

  5. TU Wien Institute of Lightweight Design and Structural Biomechanics, Vienna, Austria

    Dieter H. Pahr

  6. Department of Paleobiology, National Museum of Natural Sciences, CSIC, Madrid, Spain

    Antonio Rosas

  7. Department of Anthropology, The Pennsylvania State University, State College, PA, USA

    Nicholas B. Stephens

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  1. Christopher J. Dunmore
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Contributions

C.J.D., M.M.S. and T.L.K. conceived of and designed the study. C.J.D. collected and analysed the data. A.B. and D.H.P. contributed analysis tools. A.R., J.-J.H., L.R.B. and N.B.S. contributed data and theoretical context. C.J.D. wrote the manuscript with input from all authors.

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Correspondence to Christopher J. Dunmore.

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Extended data

Extended Data Fig. 1 Trabecular analysis method, example on Pan troglodytes metacarpus.

(a) An isosurface model of the metacarpus with inset parasagittal cross-section of the thumb metacarpal. (b) 3D isosurface showing inner trabecular structure of the metacarpus. (c) Segmented 2D cross-section of the thumb metacarpal (left), cortical and trabecular segmentation (centre), regular background grid overlaid on the isolated trabecular structure (right) and a close-up of this grid with a representation of the overlapping volumes of interest (VOIs) centred at each vertex of the background grid in purple (top). (d) Interpolation of BV/TV values, measured in overlapping VOIs, onto 3D trabecular meshes. (e) Anatomical landmarks (red), sliding semi-landmarks on curves (blue) and across the subarticular surfaces (green) on the smoothed surface of the trabecular models. (f) BV/TV values interpolated to each landmark and then divided by the mean value of each articular surface to produce RBV values on each landmark.

Extended Data Fig. 2 Cross-sectional analysis method, example on a Pongo thumb metacarpal.

(a) A parasagittal cross-section image with its manual proximo-distal axis marked in blue and the computed eigenvector that best describes this axis marked in red. (b) The 3D image is rotated by the angle between the two axes (green arrows). (c) The cross-section of the rotated image shows the eigenvector now equals the proximo-distal axis of the bone and a 50% coronal cross-section, marked in orange, is orthogonal to the new axis. The position of this 50% diaphyseal mid-slice shown in 3D (d) and the anatomical axes used to calculate directional moments of inertia are radioulnar (RU), dorsopalmar (DP). The minimum (Imin) and maximum (Imax) moments of inertia calculated for this bone are depicted (f) and were averaged to generate the average area moment of inertia (Iavg, mm4).

Extended Data Fig. 3 Extant species average distributions of subchondral RBV across the metacarpus.

(a) distal, (b) palmar and (c) dorsal views. In addition, (d) depicts the average distributions of RBV across the thumb metacarpal (Mc1) base (partially modified from46,51).

Extended Data Fig. 4 Distributions of RBV across fossil hominin metacarpi.

(a) distal, (b) palmar and (c) dorsal views. Also, (d) depicts the average distributions of RBV across the thumb metacarpal (Mc1) base and (e) displays distal, palmar, dorsal and proximal views of individual fossil thumb metacarpals.

Supplementary information

Supplementary Information

Supplementary Tables 1–7 and refs. 55–71.

Reporting Summary

Supplementary Software 1

An interactive 3D PCA depicting subchondral RBV variation across the finger metacarpals (Mc2–5). Each point represents the pattern of RBV across an associated metacarpus in one individual. Fossils are plotted in black and labelled.

Supplementary Software 2

An interactive 3D PCA depicting subchondral RBV variation across both subchondral surfaces on thumb metacarpals (Mc1). Each point represents the pattern of RBV across both subchondral surfaces in one individual. Fossils are plotted in black and labelled.

Supplementary Software 3

An interactive 3D PCA depicting subchondral RBV variation across the finger metacarpals (Mc2–4). Each point represents the pattern of RBV across an associated metacarpus in one individual. Fossils are plotted in black and labelled.

Supplementary Software 4

An interactive 3D PCA depicting subchondral RBV variation across the finger metacarpals (Mc2, 3 and 5). Each point represents the pattern of RBV across an associated metacarpus in one individual. Fossils are plotted in black and labelled.

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Dunmore, C.J., Skinner, M.M., Bardo, A. et al. The position of Australopithecus sediba within fossil hominin hand use diversity. Nat Ecol Evol 4, 911–918 (2020). https://doi.org/10.1038/s41559-020-1207-5

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