Abstract

Since the first discovery of Pithecanthropus (Homo) erectus by E. Dubois at Trinil in 1891, over 200 hominid dentognathic remains have been collected from the Early to Middle Pleistocene deposits of Java, Indonesia, forming the largest palaeoanthropological collection in South East Asia. Most of these fossils are currently attributed to H. erectus. However, because of the substantial morphological and metric variation in the Indonesian assemblage, some robust specimens, such as the partial mandibles Sangiran 5 and Sangiran 6a, were formerly variably allocated to other taxa (Meganthropus palaeojavanicus, Pithecanthropus dubius, Pongo sp.). To resolve the taxonomic uncertainty surrounding these and other contentious Indonesian hominid specimens, we used occlusal fingerprint analysis (OFA) to reconstruct their chewing kinematics; we also used various morphometric approaches based on microtomography to examine the internal dental structures. Our results confirm the presence of Meganthropus as a Pleistocene Indonesian hominid distinct from Pongo, Gigantopithecus and Homo, and further reveal that Dubois’s H. erectus paratype molars from 1891 are not hominin (human lineage), but instead are more likely to belong to Meganthropus.

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The authors declare that all data supporting the findings of this study are available within the paper and its Supplementary information files.

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References

  1. 1.

    Voris, H. K. Maps of Pleistocene sea levels in Southeast Asia: shorelines, river systems and time durations. J. Biogeogr. 27, 1153–1167 (2000).

  2. 2.

    Larick, R. & Ciochon, R. L. Early hominin biogeography in island Southeast Asia. Evol. Anthropol. 24, 185–213 (2015).

  3. 3.

    Antón, S. C., Spoor, F., Fellmann, C. D. & Swisher, C. C. in Handbook of Paleoanthropology Vol. 3 (eds Henke, W. & Tattersall, I.) 1655–1695 (Springer, 2007).

  4. 4.

    Ciochon, R. L. in Out of Africa I: the First Hominin Colonization of Eurasia (eds Fleagle, J. G. et al.) 111–126 (Springer, 2010).

  5. 5.

    Harrison, T., Jin, C., Zhang, Y., Wang, Y. & Zhu, M. Fossil Pongo from the early Pleistocene Gigantopithecus fauna of Chongzuo, Guangxi, Southern China. Quat. Int. 354, 59–67 (2014).

  6. 6.

    Zhang, Y. & Harrison, T. Gigantopithecus blacki: a giant ape from the Pleistocene of Asia revisited. Am. J. Phys. Anthropol. 162, 153–177 (2017).

  7. 7.

    Ciochon, R. L. The mystery ape of Pleistocene Asia. Nature 459, 910–911 (2009).

  8. 8.

    Ibrahim, Y. Kh. et al. First discovery of Pleistocene orangutan (Pongo sp.) fossils in Peninsular Malaysia: biogeographic and paleoenvironmental implications. J. Hum. Evol. 65, 770–797 (2013).

  9. 9.

    Kaifu, Y., Aziz, F. & Baba, H. New evidence of the existence of Pongo in the Early/Middle Pleistocene Java. In Proc. International Symposium on Geological Museum (eds Sudijono, J. & Aziz, F.) 55–60 (Geological Research and Development Centre, 2001).

  10. 10.

    Smith, T. M. et al. Taxonomic assessment of the Trinil molars using non-destructive 3D structural and development analysis. PaleoAnthropol. 2009, 117–129 (2009).

  11. 11.

    Smith, T. M. et al. Disentangling isolated dental remains of Asian Pleistocene hominins and pongines. PLoS ONE 13, e0204737 (2018).

  12. 12.

    Dubois, E. Pithecanthropus erectus, eine menschenaehnliche Ubergangsform aus Java (Landesdruckerei, 1894).

  13. 13.

    Tyler, D. E. Sangiran 5, (“Pithecanthropus dubius”), Homo erectus, “Meganthropus”, or Pongo? Hum. Evol. 18, 229–241 (2003).

  14. 14.

    von Koenigswald, G. H. R. Fossil hominids of the Lower Pleistocene of Java: Trinil. In Proc. 18th International Geological Congress 59–61 (International Geological Conference, 1950).

  15. 15.

    Weidenreich, F. Giant early man from Java and South China. Anthropol. Pap. Am. Mus. Nat. Hist. 40, 1–134 (1945).

  16. 16.

    Kaifu, Y. et al. Taxonomic affinities and evolutionary history of the Early Pleistocene hominids of Java: dentognathic evidence. Am. J. Phys. Anthropol. 128, 709–726 (2005).

  17. 17.

    Kaifu, Y., Aziz, F. & Baba, H. Hominin mandibular remains from Sangiran: 1952–1986 collection. Am. J. Phys. Anthropol. 128, 497–519 (2005).

  18. 18.

    Schwartz, J. H. & Tattersall, I. Defining the genus Homo. Science 349, 931–932 (2015).

  19. 19.

    Grimaud-Hervé, D. & Widianto, H. in Origine des peuplements et chronologie des cultures paléolithiques dans le Sud-Est asiatique (eds Sémah, F. et al.) 331–358 (Semenanjung, 2001).

  20. 20.

    Begun, D. R. A Companion to Paleoanthropology (Wiley-Blackwell, 2013).

  21. 21.

    Fleagle, J. G. Primate Adaptation and Evolution 3rd edn (Elsevier, 2013).

  22. 22.

    Teaford, M. F. & Ungar, P. S. in Handbook of Palaeoanthropology 2nd edn (eds Henke, W. & Tattersall, I.) 1465–1494 (Springer, 2015).

  23. 23.

    Kullmer, O. et al. Occlusal fingerprint analysis: quantification of tooth wear pattern. Am. J. Phys. Anthropol. 139, 600–605 (2009).

  24. 24.

    Olejniczak, A. J. et al. Molar enamel thickness and dentine horn height in Gigantopithecus blacki. Am. J. Phys. Anthropol. 135, 85–91 (2008).

  25. 25.

    Fiorenza, L., Nguyen, N. H. & Benazzi, S. Stress distribution and molar macrowear in Pongo pygmaeus: a new approach through finite element and occlusal fingerprint analyses. Hum. Evol. 30, 215–226 (2015).

  26. 26.

    Zanolli, C., Grine, F. E., Kullmer, O., Schrenk, F. & Macchiarelli, R. The early Pleistocene deciduous hominid molar FS-72 from the Sangiran Dome of Java, Indonesia: a taxonomic reappraisal based on its comparative endostructural characterization. Am. J. Phys. Anthropol. 157, 666–674 (2015).

  27. 27.

    Smith, T. M. et al. Variation in enamel thickness within the genus Homo. J. Hum. Evol. 62, 395–411 (2012).

  28. 28.

    Kupczik, K., Olejniczak, A. J., Skinner, M. M. & Hublin, J. J. Molar crown and root size relationship in anthropoid primates. Front. Oral Biol. 13, 16–22 (2009).

  29. 29.

    Skinner, M. M. et al. Dental trait expression at the enamel-dentine junction of lower molars in extant and fossil hominoids. J. Hum. Evol. 54, 173–186 (2008).

  30. 30.

    Schwartz, J. in Una vida dedicada a la ciencia y al conocimiento de los primeros europeos (ed. Ribot, R.) 93–110 (Publicaciones Diputación de Granada, 2016).

  31. 31.

    Simons, E. L. & Chopra, S. R. K. Gigantopithecus (Pongidae, Hominoidea) a new species from North India. Postilla 138, 1–18 (1969).

  32. 32.

    Wang, W. New discoveries of Gigantopithecus blacki teeth from Chuifeng Cave in the Bubing Basin, Guangxi, south China. J. Hum. Evol. 57, 229–240 (2009).

  33. 33.

    Koufos, G. D. & de Bonis, L. New material of Ouranopithecus macedoniensis from late Miocene of Macedonia (Greece) and study of its dental attrition. Géobios 39, 223–243 (2006).

  34. 34.

    Xu, Q. & Lu, Q. Lufengpithecus lufengensis: an Early Member of Hominidae (Science Press, 2007).

  35. 35.

    Smith, T. M. et al. Dental ontogeny in Pliocene and early Pleistocene hominins. PLoS ONE 10, e0118118 (2015).

  36. 36.

    Smith, T. M. Dental development in living and fossil orangutans. J. Hum. Evol. 94, 92–105 (2016).

  37. 37.

    Mahoney, P., Smith, T. M., Schwartz, G. T., Dean, C. & Kelley, J. Molar crown formation in the Late Miocene Asian hominoids, Sivapithecus parvada and Sivapithecus indicus. J. Hum. Evol. 53, 61–68 (2007).

  38. 38.

    Schwartz, G. T., Liu, W. & Zheng, L. Preliminary investigation of dental microstructure in the Yuanmou hominoid (Lufengpithecus hudienensis), Yunnan Province, China. J. Hum. Evol. 44, 189–202 (2003).

  39. 39.

    Olejniczak, A. J. et al. Three-dimensional molar enamel distribution and thickness in Australopithecus and Paranthropus. Biol. Lett. 4, 406–410 (2008).

  40. 40.

    Noerwidi, S., Siswanto, S. & Widianto, H. Giant primate of Java: a new Gigantopithecus specimen from Semedo. Berkala Arkeologi 36, 141–160 (2016).

  41. 41.

    Bettis, E. A. III et al. Way out of Africa: early Pleistocene paleoenvironments inhabited by Homo erectus in Sangiran, Java. J. Hum. Evol. 56, 11–24 (2009).

  42. 42.

    Sémah, A. M., Sémah, F., Djubiantono, T. & Brasseur, B. Landscapes and hominids’ environments: changes between the lower and the early middle Pleistocene in Java (Indonesia). Quat. Int. 223–224, 451–454 (2010).

  43. 43.

    Janssen, R. et al. Tooth enamel stable isotopes of Holocene and Pleistocene fossil fauna reveal glacial and interglacial paleoenvironments of hominins in Indonesia. Quat. Sci. Rev. 144, 145–154 (2016).

  44. 44.

    Kelley, J. & Gao, F. Juvenile hominoid cranium from the late Miocene of southern China and hominoid diversity in Asia. Proc. Natl Acad. Sci. USA 109, 6882–6885 (2012).

  45. 45.

    Ji, X.-P. et al. Juvenile hominoid cranium from the terminal Miocene of Yunnan, China. Chin. Sci. Bull. 58, 3771–3779 (2013).

  46. 46.

    Nater, A. et al. Morphometric, behavioral, and genomic evidence for a new orangutan species. Curr. Biol. 27, 3576–3577 (2017).

  47. 47.

    Kardjilov, N. et al. New features in cold neutron radiography and tomography. Part II: applied energy-selective neutron radiography and tomography. Nucl. Instrum. Methods Phys. Res. A 501, 536–546 (2003).

  48. 48.

    Tremsin, A. S. et al. High resolution neutron imaging capabilities at BOA beamline at Paul Scherrer Institut. Nucl. Instrum. Methods Phys. Res. A 784, 486–493 (2015).

  49. 49.

    Winkler, B. Applications of neutron radiography and neutron tomography. Rev. Mineral. Geochem. 63, 459–471 (2006).

  50. 50.

    Schwarz, D., Vontobel, P., Lehmann, E. H., Meyer, C. A. & Bongartz, G. Neutron tomography of internal structures of vertebrate remains: a comparison with X-ray computed tomography. Palaeontol. Electronica http://palaeo-electronica.org/2005_2/neutron/issue2_05.htm (2005).

  51. 51.

    Sutton, M. D. Tomographic techniques for the study of exceptionally preserved fossils. Proc. Biol. Sci. 275, 1587–1593 (2008).

  52. 52.

    Spoor, C. F., Zonneveld, F. W. & Macho, G. A. Linear measurements of cortical bone and dental enamel by computed tomography: applications and problems. Am. J. Phys. Anthropol. 91, 469–484 (1993).

  53. 53.

    Fajardo, R. J., Ryan, T. M. & Kappelman, J. Assessing the accuracy of high-resolution X-ray computed tomography of primate trabecular bone by comparisons with histological sections. Am. J. Phys. Anthropol. 118, 1–10 (2002).

  54. 54.

    Coleman, M. N. & Colbert, M. W. CT thresholding protocols for taking measurements on three-dimensional models. Am. J. Phys. Anthropol. 133, 723–725 (2007).

  55. 55.

    Beaudet, A. et al. Neutron microtomography-based virtual extraction and analysis of a cercopithecoid partial cranium (STS 1039) embedded in a breccia fragment from sterkfontein member 4 (South Africa). Am. J. Phys. Anthropol. 159, 737–745 (2016).

  56. 56.

    Zanolli, C. et al. Exploring hominin and non-hominin primate dental fossil remains with neutron microtomography. Physcs Proc. 88, 109–115 (2017).

  57. 57.

    Mills, J. R. E. Ideal dental occlusion in the primates. Dent. Pract. 6, 47–61 (1955).

  58. 58.

    Hiiemae, K. M. & Kay, R. F. In Proc. 4th International Congress of Primatology Vol. 3 (eds Montagna, W. & Zingeser, M. R.) 28–64 (Karger, 1973).

  59. 59.

    Kay, R. F. & Hiiemae, K. M. Jaw movement and tooth use in recent and fossil primates. Am. J. Phys. Anthropol. 40, 227–256 (1974).

  60. 60.

    Maier, W. & Schneck, G. Konstruktionsmorphologische Untersuchungen am Gebiß der hominoiden Primaten. Z. Morphol. Anthropol. 72, 127–169 (1981).

  61. 61.

    Ulhaas, L., Kullmer, O. & Schrenk, F. in Dental Perspectives on Human Evolution: State of the Art Research in Dental Paleoanthropology (eds Bailey, S. E. & Hublin, J. J.) 369–390 (Springer, 2007).

  62. 62.

    Kullmer, O., Schulz, D. & Benazzi, S. An experimental approach to evaluate the correspondence between wear facet position and occlusal movements. Anat. Rec. (Hoboken) 295, 846–852 (2012).

  63. 63.

    von Koenigswald, W., Anders, U., Engels, S., Schultz, J. A. & Kullmer, O. Jaw movement in fossil mammals: analysis, description and visualization. Palaontol. Z. 87, 141–159 (2013).

  64. 64.

    Fiorenza, L. et al. Molar macrowear reveals Neanderthal ecogeographic dietary variation. PLoS ONE 6, e14769 (2011).

  65. 65.

    Janis, C. M. in Evolutionary Paleobiology of Behavior and Coevolution (ed. Boucot, A. J.) 241–259 (Elsevier, 1990).

  66. 66.

    Hamilton, N. ggtern: An extension to ‘ggplot2’, for the creation of ternary diagrams. R version 2.2.2 https://CRAN.R-project.org/package=ggtern (2017).

  67. 67.

    R Core Team. R: a Language and Environment for Statistical computing (R Foundation for Statistical Computing, 2017).

  68. 68.

    Hervé, M. RVAideMemoire: Diverse basic statistical and graphical functions. R version 0.9-66 https://CRAN.R-project.org/package=RVAideMemoire (2017).

  69. 69.

    Olejniczak, A. J. et al. Dental tissue proportions and enamel thickness in Neandertal and modern human molars. J. Hum. Evol. 55, 12–23 (2008).

  70. 70.

    Kupczik, K. & Dean, M. C. Comparative observations on the tooth root morphology of Gigantopithecus blacki. J. Hum. Evol. 54, 196–204 (2008).

  71. 71.

    Maureille, B., Rougier, H., Houët, F. & Vandermeersch, B. Les dents inférieures du néandertalien Regourdou 1 (site de Regourdou, commune de Montignac, Dordogne): analyses métriques et comparatives. Paléo 13, 183–200 (2001).

  72. 72.

    Scolan, H., Santos, F., Tillier, A. M., Maureille, B. & Quintard, A. Des nouveaux vestiges néanderthaliens à Las Pélénos (Monsempron-Libos, Lot-et-Garonne, France). Bull. Mem. Soc. Anthropol. Paris 24, 69–95 (2012).

  73. 73.

    Macchiarelli, R., Bondioli, L. & Mazurier, A. in Technique and Application in Dental Anthropology (eds Irish, J. D. & Nelson, G. C.) 426–448 (Cambridge Univ. Press, 2008).

  74. 74.

    Macchiarelli, R., Bayle, P., Bondioli, L., Mazurier, A. & Zanolli, C. in Anthropological Perspectives on Tooth Morphology. Genetics, Evolution, Variation (eds Scott, G. R. & Irish, J. D.) 250–277 (Cambridge Univ. Press, 2013).

  75. 75.

    Bayle, P. et al. in Pleistocene Databases. Acquisition, Storing, Sharing (eds Macchiarelli, R. & Weniger, G. C.) 29–46 (Neanderthal Museums, 2011).

  76. 76.

    Zanolli, C., Bayle, P. & Macchiarelli, R. Tissue proportions and enamel thickness distribution in the early Middle Pleistocene human deciduous molars from Tighenif (Ternifine), Algeria. C. R. Palevol. 9, 341–348 (2010).

  77. 77.

    Zanolli, C. Molar crown inner structural organization in Javanese Homo erectus. Am. J. Phys. Anthropol. 156, 148–157 (2015).

  78. 78.

    Mitteroecker, P. & Bookstein, F. L. Linear discrimination, ordination, and the visualization of selection gradients in modern morphometrics. Evol. Biol. 38, 100–114 (2011).

  79. 79.

    Dray, S. & Dufour, A. B. The ade4 package: implementing the duality diagram for ecologists. J. Stat. Softw. 22, 1–20 (2007).

  80. 80.

    Bookstein, F. L. Morphometric Tools for Landmark Data: Geometry and Biology (Cambridge Univ. Press, 1991).

  81. 81.

    Gokcen, I. & Peng, J. Comparing linear discriminant analysis and support vector machines. In Proc. Advances in Information Systems: Second International Conference, ADVIS 2002 (ed. Yakhno, T.) 104–113 (Springer, 2002).

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Acknowledgements

We thank the Pusat Penelitian Arkeologi of Jakarta and the Balai Pelestarian Situs Manusia Purba of Sangiran, Java, and the Muséum national d’histoire naturelle. We thank the many curators and colleagues who granted access to fossil and recent hominid materials for scanning. We are grateful to D. Grimaud-Hervé, C. Hertler, F. Sémah and H. Widianto for their support. We thank J. Braga for sharing the microtomographic scans of South African fossil specimens. For scientific discussion, we thank P. Bayle, S. Benazzi, L. Bondioli, J. Braga, M.C. Dean, F. Détroit, Y. Hou, L. Mancini, B. Maureille, A. Mazurier, L. Puymerail, L. Rook, C. Tuniz and B. Wood. We would like to express our gratitude to C. Hemm, L. Hauser, M. Janocha and L. Strzelczyk for their help with the surface scanning and OFA analysis. Scanning of the Vietnamese specimens was funded by the Projet International de Coopération Scientifique-Centre national de la recherche scientifique (CNRS) grant to A.M.B (PICS 2011-2013 n°5712). Research was supported by the CNRS.

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Affiliations

  1. Laboratoire PACEA, UMR 5199 CNRS, Université de Bordeaux, Pessac, France

    • Clément Zanolli
  2. Laboratoire AMIS, UMR 5288 CNRS, Université Toulouse III Paul Sabatier, Toulouse, France

    • Clément Zanolli
    •  & Jean Dumoncel
  3. Department of Palaeoanthropology, Senckenberg Research Institute and Natural History Museum Frankfurt, Frankfurt am Main, Germany

    • Ottmar Kullmer
    •  & Friedemann Schrenk
  4. Department of Paleobiology and Environment, Institute of Ecology, Evolution, and Diversity, Goethe University, Frankfurt, Germany

    • Ottmar Kullmer
    •  & Friedemann Schrenk
  5. Institute of Human Origins and School of Human Evolution and Social Change, Arizona State University, AZ, Tempe, USA

    • Jay Kelley
  6. Department of Paleobiology, National Museum of Natural History, Smithsonian Institution, Washington, DC, USA

    • Jay Kelley
  7. Department of Human Evolutionary Biology, Harvard University, MA, Cambridge, USA

    • Jay Kelley
  8. Laboratoire BABEL, FRE 2029 CNRS, Université Paris Descartes, Faculté de chirurgie dentaire, Montrouge, France

    • Anne-Marie Bacon
  9. Lundbeck Foundation GeoGenetics Center, Copenhagen, Denmark

    • Fabrice Demeter
  10. UMR 7206 CNRS, Muséum national d’histoire naturelle, Paris, France

    • Fabrice Demeter
  11. Department of Anatomy and Developmental Biology, Monash University, Victoria, Melbourne, Australia

    • Luca Fiorenza
  12. Earth Sciences, University of New England, New South Wales, Armidale, Australia

    • Luca Fiorenza
  13. Department of Anthropology and Department of Anatomical Sciences, Stony Brook University, NY, Stony Brook, USA

    • Frederick E. Grine
  14. Department of Human Evolution, Max Planck Institute for Evolutionary Anthropology, Leipzig, Germany

    • Jean-Jacques Hublin
    •  & Matthew M. Skinner
  15. Anthropological and Palaeoenvironmental Department, The Institute of Archaeology, Hanoi, Vietnam

    • Anh Tuan Nguyen
    •  & Thi Mai Huong Nguyen
  16. Key Laboratory of Vertebrate Evolution and Human Origins, Institute of Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Sciences, Beijing, China

    • Lei Pan
  17. State Key Laboratory of Palaeobiology and Stratigraphy, Nanjing Institute of Geology and Palaeontology, Chinese Academy of Sciences, Nanjing, China

    • Lei Pan
  18. Heinz Maier-Leibnitz Center (FRM-II), Technische Universität München, Garching, Germany

    • Burkhard Schillinger
  19. School of Anthropology and Conservation, University of Kent, Canterbury, UK

    • Matthew M. Skinner
  20. Department of Paleoanthropology, Yunnan Institute of Cultural Relics and Archaeology, Kunming, China

    • Xueping Ji
  21. School of Resource Environment and Earth Science, Yunnan University, Kunming, China

    • Xueping Ji
  22. UMR 7194 CNRS, Muséum national d’histoire naturelle, Paris, France

    • Roberto Macchiarelli
  23. Unité de Formation Géosciences, Université de Poitiers, Poitiers, France

    • Roberto Macchiarelli

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Contributions

The study was initiated by C.Z. during his PhD research project under the supervision of R.M. Microtomography-based data were collected and elaborated by C.Z., A.M.B., F.D., J.K., O.K., L.F., F.S., A.T.N., T.M.H.N., B.S., J.-J.H., M.M.S., X.J. and R.M. Quantitative data were compiled and analysed by C.Z., J.D., O.K., L.F., L.P., M.M.S., F.E.G. and R.M. C.Z, R.M, O.K. and J.K. wrote the manuscript with contributions from all the other authors.

Competing interests

The authors declare no competing interests.

Corresponding author

Correspondence to Clément Zanolli.

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https://doi.org/10.1038/s41559-019-0860-z