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Enamel proteins reveal biological sex and genetic variability within southern African Paranthropus

View ORCID ProfilePalesa P. Madupe, View ORCID ProfileClaire Koenig, View ORCID ProfileIoannis Patramanis, View ORCID ProfilePatrick L. Rüther, Nomawethu Hlazo, Meaghan Mackie, Mirriam Tawane, View ORCID ProfileJohanna Krueger, View ORCID ProfileAlberto J. Taurozzi, Gaudry Troché, Job Kibii, Robyn Pickering, Marc Dickinson, View ORCID ProfileYonatan Sahle, Dipuo Kgotleng, Charles Musiba, Fredrick Manthi, Liam Bell, Michelle DuPlessis, View ORCID ProfileCatherine Gilbert, Bernhard Zipfel, Lukas F. K. Kuderna, View ORCID ProfileEsther Lizano, View ORCID ProfileFrido Welker, Pelagia Kyriakidou, Jürgen Cox, Catherine Mollereau, Caroline Tokarski, Jonathan Blackburn, View ORCID ProfileJazmín Ramos-Madrigal, Tomas Marques-Bonet, Kirsty Penkman, Clément Zanolli, View ORCID ProfileLauren Schroeder, View ORCID ProfileFernando Racimo, View ORCID ProfileJesper V. Olsen, View ORCID ProfileRebecca R. Ackermann, View ORCID ProfileEnrico Cappellini
doi: https://doi.org/10.1101/2023.07.03.547326
Palesa P. Madupe
1Geogenetics Section, Globe institute, University of Copenhagen, Denmark
2Human Evolution Research Institute (HERI), University of Cape Town, Cape Town, South Africa
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Claire Koenig
3Novo Nordisk Foundation Center for Protein Research, University of Copenhagen, Denmark
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  • ORCID record for Claire Koenig
Ioannis Patramanis
4Section for Molecular Ecology and Evolution, Globe Institute, University of Copenhagen, Denmark
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  • ORCID record for Ioannis Patramanis
Patrick L. Rüther
3Novo Nordisk Foundation Center for Protein Research, University of Copenhagen, Denmark
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Nomawethu Hlazo
5Department of Archaeology, University of Cape Town, Cape Town, South Africa
2Human Evolution Research Institute (HERI), University of Cape Town, Cape Town, South Africa
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Meaghan Mackie
1Geogenetics Section, Globe institute, University of Copenhagen, Denmark
3Novo Nordisk Foundation Center for Protein Research, University of Copenhagen, Denmark
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Mirriam Tawane
6Plio-Pleistocene Palaeontology Section, Ditsong National Museum of Natural History, Pretoria, South Africa
2Human Evolution Research Institute (HERI), University of Cape Town, Cape Town, South Africa
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Johanna Krueger
7Institute of Evolutionary Biology (UPF-CSIC), PRBB, Barcelona, Spain
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Alberto J. Taurozzi
1Geogenetics Section, Globe institute, University of Copenhagen, Denmark
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Gaudry Troché
1Geogenetics Section, Globe institute, University of Copenhagen, Denmark
3Novo Nordisk Foundation Center for Protein Research, University of Copenhagen, Denmark
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Job Kibii
8Turkana Basin Institute, Nairobi, Kenya
2Human Evolution Research Institute (HERI), University of Cape Town, Cape Town, South Africa
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Robyn Pickering
9Department of Geological Sciences, University of Cape Town, Cape Town, South Africa
2Human Evolution Research Institute (HERI), University of Cape Town, Cape Town, South Africa
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Marc Dickinson
10Department of Chemistry, University of York, York, United Kingdom
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Yonatan Sahle
5Department of Archaeology, University of Cape Town, Cape Town, South Africa
2Human Evolution Research Institute (HERI), University of Cape Town, Cape Town, South Africa
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Dipuo Kgotleng
11Palaeo-Research Institute, University of Johannesburg, Johannesburg, South Africa
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Charles Musiba
12Department of Anthropology, University of Colorado Denver, Colorado, United States of America
2Human Evolution Research Institute (HERI), University of Cape Town, Cape Town, South Africa
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Fredrick Manthi
13Palaeontology Section, National Museums of Kenya, Nairobi, Kenya
2Human Evolution Research Institute (HERI), University of Cape Town, Cape Town, South Africa
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Liam Bell
14D-CYPHR, Centre for Proteomic and Genomic Research, Cape Town, South Africa
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Michelle DuPlessis
14D-CYPHR, Centre for Proteomic and Genomic Research, Cape Town, South Africa
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Catherine Gilbert
15CBMN, UMR CNRS 5248, Proteome Platform, University of Bordeaux, Bordeaux, France
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  • ORCID record for Catherine Gilbert
Bernhard Zipfel
16Evolutionary Studies Institute, University of the Witwatersrand, Johannesburg, South Africa
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Lukas F. K. Kuderna
7Institute of Evolutionary Biology (UPF-CSIC), PRBB, Barcelona, Spain
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Esther Lizano
7Institute of Evolutionary Biology (UPF-CSIC), PRBB, Barcelona, Spain
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Frido Welker
4Section for Molecular Ecology and Evolution, Globe Institute, University of Copenhagen, Denmark
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Pelagia Kyriakidou
17Computational Systems Biochemistry, Max Planck Institute of Biochemistry, Martinsried, Germany
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Jürgen Cox
17Computational Systems Biochemistry, Max Planck Institute of Biochemistry, Martinsried, Germany
18Department of Biological and Medical Psychology, University of Bergen, Bergen, Norway
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Catherine Mollereau
19Research Center on Animal Cognition (CRCA), Center of Integrative Biology (CBI), University of Toulouse, CNRS UMR-5169, UPS, Toulouse, France
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Caroline Tokarski
15CBMN, UMR CNRS 5248, Proteome Platform, University of Bordeaux, Bordeaux, France
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Jonathan Blackburn
20Institute of Infectious Disease and Molecular Medicine, University of Cape Town, Cape Town, South Africa
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Jazmín Ramos-Madrigal
21Section for Molecular Ecology and Evolution, Globe Institute, University of Copenhagen, Denmark
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Tomas Marques-Bonet
7Institute of Evolutionary Biology (UPF-CSIC), PRBB, Barcelona, Spain
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Kirsty Penkman
10Department of Chemistry, University of York, York, United Kingdom
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Clément Zanolli
22Univ. Bordeaux, CNRS, MCC, PACEA, UMR 5199, F-33600 Pessac, France
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Lauren Schroeder
23Department of Anthropology, University of Toronto Mississauga, Canada
2Human Evolution Research Institute (HERI), University of Cape Town, Cape Town, South Africa
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Fernando Racimo
4Section for Molecular Ecology and Evolution, Globe Institute, University of Copenhagen, Denmark
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Jesper V. Olsen
3Novo Nordisk Foundation Center for Protein Research, University of Copenhagen, Denmark
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  • For correspondence: jesper.olsen@cpr.ku.dk becky.ackermann@uct.ac.za ecappellini@sund.ku.dk
Rebecca R. Ackermann
5Department of Archaeology, University of Cape Town, Cape Town, South Africa
2Human Evolution Research Institute (HERI), University of Cape Town, Cape Town, South Africa
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  • For correspondence: jesper.olsen@cpr.ku.dk becky.ackermann@uct.ac.za ecappellini@sund.ku.dk
Enrico Cappellini
1Geogenetics Section, Globe institute, University of Copenhagen, Denmark
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  • For correspondence: jesper.olsen@cpr.ku.dk becky.ackermann@uct.ac.za ecappellini@sund.ku.dk
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Abstract

The evolutionary relationships among extinct African hominin taxa are highly debated and largely unresolved, due in part to a lack of molecular data. Even within taxa, it is not always clear, based on morphology alone, whether ranges of variation are due to sexual dimorphism versus potentially undescribed taxonomic diversity. For Paranthropus robustus, a Pleistocene hominin found only in South Africa, both phylogenetic relationships to other taxa 1,2 and the nature of intraspecific variation 3–6 are still disputed. Here we report the mass spectrometric (MS) sequencing of enamel proteomes from four ca. 2 million year (Ma) old dental specimens attributed morphologically to P. robustus, from the site of Swartkrans. The identification of AMELY-specific peptides and semi-quantitative MS data analysis enabled us to determine the biological sex of all the specimens. Our combined molecular and morphometric data also provide compelling evidence of a significant degree of variation within southern African Paranthropus, as previously suggested based on morphology alone 6. Finally, the molecular data also confirm the taxonomic placement of Paranthropus within the hominin clade. This study demonstrates the feasibility of recovering informative Early Pleistocene hominin enamel proteins from Africa. Crucially, it also shows how the analysis of these proteins can contribute to understanding whether hominin morphological variation is due to sexual dimorphism or to taxonomic differences. We anticipate that this approach can be widely applied to geologically-comparable sites within South Africa, and possibly more broadly across the continent.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • ↵# Lukas F. K. Kuderna is currently an employee of Illumina Inc.

  • https://github.com/ClaireKoenig/ProteinSequenceAssembly

  • https://github.com/johnpatramanis/Code_for_Genetic_Diversity_Sampling

  • https://proteomecentral.proteomexchange.org/cgi/GetDataset?ID=PXD040221

  • https://zenodo.org/record/7801259

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Enamel proteins reveal biological sex and genetic variability within southern African Paranthropus
Palesa P. Madupe, Claire Koenig, Ioannis Patramanis, Patrick L. Rüther, Nomawethu Hlazo, Meaghan Mackie, Mirriam Tawane, Johanna Krueger, Alberto J. Taurozzi, Gaudry Troché, Job Kibii, Robyn Pickering, Marc Dickinson, Yonatan Sahle, Dipuo Kgotleng, Charles Musiba, Fredrick Manthi, Liam Bell, Michelle DuPlessis, Catherine Gilbert, Bernhard Zipfel, Lukas F. K. Kuderna, Esther Lizano, Frido Welker, Pelagia Kyriakidou, Jürgen Cox, Catherine Mollereau, Caroline Tokarski, Jonathan Blackburn, Jazmín Ramos-Madrigal, Tomas Marques-Bonet, Kirsty Penkman, Clément Zanolli, Lauren Schroeder, Fernando Racimo, Jesper V. Olsen, Rebecca R. Ackermann, Enrico Cappellini
bioRxiv 2023.07.03.547326; doi: https://doi.org/10.1101/2023.07.03.547326
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Enamel proteins reveal biological sex and genetic variability within southern African Paranthropus
Palesa P. Madupe, Claire Koenig, Ioannis Patramanis, Patrick L. Rüther, Nomawethu Hlazo, Meaghan Mackie, Mirriam Tawane, Johanna Krueger, Alberto J. Taurozzi, Gaudry Troché, Job Kibii, Robyn Pickering, Marc Dickinson, Yonatan Sahle, Dipuo Kgotleng, Charles Musiba, Fredrick Manthi, Liam Bell, Michelle DuPlessis, Catherine Gilbert, Bernhard Zipfel, Lukas F. K. Kuderna, Esther Lizano, Frido Welker, Pelagia Kyriakidou, Jürgen Cox, Catherine Mollereau, Caroline Tokarski, Jonathan Blackburn, Jazmín Ramos-Madrigal, Tomas Marques-Bonet, Kirsty Penkman, Clément Zanolli, Lauren Schroeder, Fernando Racimo, Jesper V. Olsen, Rebecca R. Ackermann, Enrico Cappellini
bioRxiv 2023.07.03.547326; doi: https://doi.org/10.1101/2023.07.03.547326

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