The phylogenetic status of Homo heidelbergensis – a cladistic study of Middle Pleistocene hominins

Le statut phylogénétique d’Homo heidelbergensis – étude cladistique des homininés du Pléistocène moyen

Abstract

Two views prevail concerning the significance of H. heidelbergensis in Middle Pleistocene human evolution. H. heidelbergensis sensu stricto refers to a European chronospecies of H. neanderthalensis while H. heidelbergensis sensu lato is considered to be an Afro-European species ancestral to modern humans and Neandertals.

Here, we test the phylogenetic validity of H. heidelbergensis using a cladistic analysis based on cranial morphological data of Pleistocene fossils. We perform a low-level analysis to ascertain the information content of the morphological features, a high-level analysis with reweighted characters resulting in a single most parsimonious cladogram and a bootstrap analysis to assess the robustness of this cladogram.

Our results show that (i) the identification of a coherent H. heidelbergensis s.l. species is not well supported and is equivocal; (ii) the hypothetical last common ancestor of H. sapiens and H. neanderthalensis has more affinities with African specimens than European; (iii) two Middle Pleistocene European fossils (Atapuerca SH5 and Steinheim) should be classified as H. neanderthalensis.

Résumé

Le rôle d’Homo heidelbergensis dans l’évolution humaine au Pléistocène moyen est interprété à la lumière de deux hypothèses principales. H. heidelbergensis sensu stricto fait référence à une chrono-espèce européenne d’Homo neanderthalensis alors que H. heidelbergensis sensu lato est considérée comme l’espèce afro-européenne ancestrale aux hommes modernes et aux Néandertaliens.

Dans cette étude, nous testons la validité phylogénétique d’H. heidelbergensis à l’aide d’une analyse cladistique basée sur des caractères morphologiques crâniens de fossiles du Pléistocène. Nous réalisons une analyse de premier ordre (‘low-level’) pour quantifier le contenu d’information des caractères morphologiques; puis une analyse de deuxième ordre (‘high-level’), avec des caractères pondérés, permettant l’obtention d’un unique cladogramme le plus parcimonieux et finalement une analyse bootstrap afin d’évaluer la robustesse de ce cladogramme.

Nos résultats montrent que (i) l’identification d’une espèce cohésive H. heidelbergensis s.l. n’est pas bien étayée et est donc équivoque; (ii) le dernier ancêtre commun hypothétique à H. sapiens et H. neanderthalensis a plus d’affinité avec les fossiles africains qu’européens; (iii) deux fossiles du Pléistocène moyen (Atapuerca SH5 et Steinheim) devraient être classé en tant qu’H. neanderthalensis.

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References

  1. 1.

    Schoetensack, O. (1908) Der Unterkiefer des Homo heidelbergensis aus den Sanden von Mauer bei Heidelberg. Leipzig: Wilhelm Engelmann. 67 p

    Google Scholar 

  2. 2.

    Rightmire, G.P. (2008) Homo in the middle Pleistocene: Hypodigms, variation, and species recognition. Evol Anthrop 17:8–21

    Article  Google Scholar 

  3. 3.

    Manzi, G. (2011) Before the Emergence of Homo sapiens: Overview on the Early-to-Middle Pleistocene Fossil Record (with a Proposal about Homo heidelbergensis at the subspecific level). Int J Evol Biol 2011:582678

    PubMed Central  PubMed  Article  Google Scholar 

  4. 4.

    Stringer, C. (2012) The status of Homo heidelbergensis (Schoetensack 1908). Evol Anthrop 21:101–07

    Article  Google Scholar 

  5. 5.

    Wagner, G.A., et al (2010) Radiometric dating of the type-site for Homo heidelbergensis at Mauer, Germany. Proceed Natl Acad Sci USA 107:19726–30

    CAS  Article  Google Scholar 

  6. 6.

    Martinon-Torres, M., et al (2012) Morphological description and comparison of the dental remains from Atapuerca-Sima de los Huesos site (Spain). J Hum Evol 62:7–58

    PubMed  Article  Google Scholar 

  7. 7.

    Mounier, A., F. Marchal, and S. Condemi (2009) Is Homo heidelbergensis a distinct species? New insight on the Mauer mandible. J Hum Evol 56:219–46

    PubMed  Article  Google Scholar 

  8. 8.

    Rosas, A. and J. M. Bermúdez de Castro (1998) The Mauer mandible and the evolutionary significance of Homo heidelbergensis. Geobios 31:687–97

    Article  Google Scholar 

  9. 9.

    Kraatz, R. (1985) A review of recent research on Heidelberg man, Homo erectus heidelbergensis. In: E. Delson, Editor Ancestors: The Hard Evidence. Alan R. Liss, Inc.: New York. pp 268–71

    Google Scholar 

  10. 10.

    Campbell, B.G. (1964) Quantitative taxonomy and human evolution. In: S. L. Washburn, Editor Classification and Human Evolution. Methuen and Co Ltd.: London. pp 50–74

    Google Scholar 

  11. 11.

    Caparros, M. (1997) Homo sapiens archaïques: un ou plusieurs taxons (espèces)? Analyse cladistique et analyse morphomé trique. Thèse du Muséum national d’Histoire naturelle. pp. 262

    Google Scholar 

  12. 12.

    Rightmire, G.P. (1998) Human evolution in the Middle Pleistocene: The role of Homo heidelbergensis. Evol Anthrop 6:218–27

    Article  Google Scholar 

  13. 13.

    Tattersall, I. (2000) Paleoanthropology: the last half-century. Evol Anthrop 9:2–16

    Article  Google Scholar 

  14. 14.

    Arsuaga, J.L., et al (1997) The Sima de los Huesos crania (Sierra de Atapuerca, Spain). A comparative study. J Hum Evol 33:219–81

    CAS  PubMed  Article  Google Scholar 

  15. 15.

    Stringer, C.B. (1992) Replacement, continuity and the origin of Homo sapiens. In: G. Bräuer and F. H. Smith, Editors Continuity or replacement. Controversies in Homo sapiens evolution. A. A. Balkema: Rotterdam / Brookfield. pp 9–24

    Google Scholar 

  16. 16.

    Reich, D., et al (2011) Denisova Admixture and the First Modern Human Dispersals into Southeast Asia and Oceania. Am J Hum Genet 89:516–28

    PubMed Central  CAS  PubMed  Article  Google Scholar 

  17. 17.

    Fu, Q., et al (2014) Genome sequence of a 45,000-year-old modern human from western Siberia. Nature 514:445–49

    CAS  PubMed  Article  Google Scholar 

  18. 18.

    Prufer, K., et al (2014) The complete genome sequence of a Neanderthal from the Altai Mountains. Nature 505:43–9

    PubMed Central  PubMed  Article  CAS  Google Scholar 

  19. 19.

    Reich, D., et al (2010) Genetic history of an archaic hominin group from Denisova Cave in Siberia. Nature 468:1053–60

    PubMed Central  CAS  PubMed  Article  Google Scholar 

  20. 20.

    Condemi, S. (1989) Décalage dans l’apparition des traits néanderthaliens sur le crâne cérébral chez les fossiles du Riss-W ürm. In: G. Giacobini, Editor Hominidae. Jaca Book: Milano. pp 357–62

    Google Scholar 

  21. 21.

    Dean, D., et al (1998) On the phylogenetic position of the pre- Neandertal specimen from Reilingen, Germany. J Hum Evol 34:485–508

    CAS  PubMed  Article  Google Scholar 

  22. 22.

    Hublin, J.-J. (1988) Les plus anciens représentants de la lignée prénéandertalienne. In: E. Trinkaus, Editor L’Homme de Néandertal. Volume 3, l’anatomie. Université de Liège: Liège. pp 81–94

    Google Scholar 

  23. 23.

    Hublin, J.-J. (1988) Les présapiens européens. In: E. Trinkaus, Editor L’Homme de Néandertal. Volume 3, l’anatomie. Université de Liège: Liège. pp 75–80

    Google Scholar 

  24. 24.

    Hublin, J.-J. (2009) The origin of Neandertals. P Natl Acad Sci USA 106:16022–27

    CAS  Article  Google Scholar 

  25. 25.

    Woodward, A.S. (1921) A new cave man from Rhodesia, South Africa. Nature 108:371–72

    Article  Google Scholar 

  26. 26.

    Mayr, E. and P. D. Aschlock (1991) Principles of systematic biology. New York: McGraw-Hillp

    Google Scholar 

  27. 27.

    Stringer, C.B. (1983) Some further notes on the morphology and dating of the Petralona hominid. J Hum Evol 12:731–42

    Article  Google Scholar 

  28. 28.

    Mounier, A. (2009) Validité du taxon Homo heidelbergensis Schoetensack, 1908.Thèse de l’Université de la Méditerrannée. Faculté de Médecine de Marseille. pp. 514

    Google Scholar 

  29. 29.

    Mounier, A. (2011) Définition du taxon Homo heidelbergensis Schoetensack, 1908: analyse phénétique du massif facial supérieur des fossiles du genre Homo du Pléistocène moyen Bull Mém Soc Anthrop Paris 23:115–51

    Google Scholar 

  30. 30.

    Rightmire, G.P. (1996) The human cranium from Bodo, Ethiopia: Evidence for speciation in the Middle Pleistocene? J Hum Evol 31:21–39

    Article  Google Scholar 

  31. 31.

    Carbonell, E., et al (1995) Lower Pleistocene hominids and artifacts from Atapuerca-TD6 (Spain). Science 269:826–30

    CAS  PubMed  Article  Google Scholar 

  32. 32.

    Carbonell, E., et al (2008) The first hominin of Europe. Nature 452:465–69

    CAS  PubMed  Article  Google Scholar 

  33. 33.

    Krause, J., et al (2010) The complete mitochondrial DNA genome of an unknown hominin from southern Siberia. Nature 464:894–97

    CAS  PubMed  Article  Google Scholar 

  34. 34.

    Meyer, M., et al (2014) A mitochondrial genome sequence of a hominin from Sima de los Huesos. Nature 505(7483):403–406

    CAS  PubMed  Article  Google Scholar 

  35. 35.

    Bermúdez de Castro, J.M., et al (2011) Early Pleistocene human mandible from Sima del Elefante (TE) cave site in Sierra de Atapuerca (Spain): A comparative morphological study. J Hum Evol 61(1):12–25

    Article  Google Scholar 

  36. 36.

    Bermúdez de Castro, J.M., et al (2007) Comparative analysis of the Gran Dolina-TD6 (Spain) and Tighenif (Algeria) Hominin mandibles. Bull Mém Soc Anthrop Paris 19(3–4):149–167

    Google Scholar 

  37. 37.

    Martinón-Torres, M., et al (2007) Dental evidence on the hominin dispersals during the Pleistocene. P Natl Acad Sci USA 104(33): 13279–13282

    Article  CAS  Google Scholar 

  38. 38.

    Trinkaus, E. (1988) The evolutionary origins of the Neandertals or, why were there Neandertals? In: E. Trinkaus, Editor L’Homme de Neandertal. Volume 3, l’Anatomie. Université de Liège: Liège. pp 11–29

    Google Scholar 

  39. 39.

    Hublin, J.-J. (1988) Caractères dérivés de la région occipitomastoïdienne chez les néandertaliens. In: E. Trinkaus, Editor L’homme de Néandertal. Volume 3, l’anatomie. Université de Liège: Liège. pp 67–73

    Google Scholar 

  40. 40.

    Condemi, S. (1992) Les Hommes Fossiles de Saccopastore et leurs Relations Phylogénétiques. Cahier de Paléoanthropologie. Paris: CNRS Editions. 169 p

    Google Scholar 

  41. 41.

    Mounier, A., S. Condemi, and G. Manzi (2011) The Stem Species of Our Species: A Place for the Archaic Human Cranium from Ceprano, Italy. PLoS ONE 6(4):e18821

    PubMed Central  CAS  PubMed  Article  Google Scholar 

  42. 42.

    Zeitoun, V. (2000) Révision de l’espèce Homo erectus (Dubois, 1893). Utilisation des données morphologiques et métriques en cladistique, reconsidération du cas Homo erectus. Bull Mém Soc Anthrop Paris 12(1–2):1–200

    Google Scholar 

  43. 43.

    Zeitoun, V. (2001) The taxinomical position of the skull of Zuttiyeh.Comptes Rendus de l’Académie des Sciences - Series IIA - Earth and Planetary Science. 332(8): 521–525

    Google Scholar 

  44. 44.

    Asfaw, B., et al (2002) Remains of Homo erectus from Bouri, Middle Awash, Ethiopia. Nature 416:317–320

    PubMed  Article  Google Scholar 

  45. 45.

    Gilbert, W.H., T. D. White, and B. Asfaw (2003) Homo erectus, Homo ergaster, Homo “cepranensis,” and the Daka cranium. J Hum Evol 45(3):255–259

    PubMed  Article  Google Scholar 

  46. 46.

    Mallegni, F., et al (2003) Homo cepranensis sp. nov. and the evolution of African-European Middle Pleistocene hominids. C R Palevol 2:153–9

    Article  Google Scholar 

  47. 47.

    Prat, S. (2004) Les premiers représentants du genre Homo, en quête d’une identité. Apports de l’étude morphologique et de l’analyse cladistique. Bull Mém Soc Anthrop Paris 16(1–2):17–35

    Google Scholar 

  48. 48.

    Zeitoun, V. (1996) Cladistique et Paleoanthropologie: le cas de l’espèce Homo erectus (Dubois, 1894).Thèse de l’Université des Sciences de Bordeaux I. pp. 344

    Google Scholar 

  49. 49.

    Prat, S. (2002) Anatomical study of the skull of the Kenyan specimen KNM-ER 1805: a re-evaluation of its taxonomic allocation? C R Palevol 1(1):27–33

    Article  Google Scholar 

  50. 50.

    Widianto, H. and V. Zeitoun (2003) Morphological description, biometry phylogenetic position of the skull of Ngawi 1 (East Java, Indonesia). Int J Osteoarchaeol 13:339–351

    Article  Google Scholar 

  51. 51.

    Gonzalez-Jose, R., et al (2008) Cladistic analysis of continuous modularized traits provides phylogenetic signals in Homo evolution. Nature 453(7196):775–778

    CAS  PubMed  Article  Google Scholar 

  52. 52.

    Zeitoun, V., et al (2010) Solo man in question: Convergent views to split Indonesian Homo erectus in two categories. Quatern Int 223–224(0):281–292

    Article  Google Scholar 

  53. 53.

    Stringer, C.B. (1987) A numerical cladistic analysis for the genus Homo. J Hum Evol 16(1):135–146

    Article  Google Scholar 

  54. 54.

    Lordkipanidze, D., et al (2013) A Complete Skull from Dmanisi, Georgia, and the Evolutionary Biology of Early Homo. Science 342(6156):326–331

    CAS  PubMed  Article  Google Scholar 

  55. 55.

    Schwartz, J.H., I. Tattersall, and Z. Chi (2014) Comment on “A Complete Skull from Dmanisi, Georgia, and the Evolutionary Biology of Early Homo”. Science 344(6182):360

    CAS  PubMed  Article  Google Scholar 

  56. 56.

    Zollikofer, C.P.E., et al (2014) Response to Comment on “A Complete Skull from Dmanisi, Georgia, and the Evolutionary Biology of Early Homo”. Science 344(6182):360

    CAS  PubMed  Article  Google Scholar 

  57. 57.

    de Lumley, M.A., et al (2006) Les restes humains du Pliocène final et du début du Pléistocène inférieur de Dmanissi, Géorgie (1991–2000). I–Les crânes, D 2280, D 2282, D 2700. L’Anthropologie 110:1–110

    Article  Google Scholar 

  58. 58.

    Gathogo, P. N. and F. H. Brown (2006) Revised stratigraphy of Area 123, Koobi Fora, Kenya, and new age estimates of its fossil mammals, including hominins. J Hum Evol 51(5):471–9

    PubMed  Article  Google Scholar 

  59. 59.

    Larick, R., et al (2001) Early Pleistocene 40Ar/39Ar ages for Bapang Formation hominins, Central Java, Indonesia. P Natl Acad Sci USA 98(9):4866–4871

    CAS  Article  Google Scholar 

  60. 60.

    Arnold, L.J., et al (2014) Luminescence dating and palaeomagnetic age constraint on hominins from Sima de los Huesos, Atapuerca, Spain. J Hum Evol 67(0):85–107

    PubMed  Article  Google Scholar 

  61. 61.

    Yokoyama, Y. (1989) Direct gamma-ray spectrometric dating of anteneandertalian and neandertalian human remains. In: G. Giacobini, Editor Hominidae. Proceedings of the second international Congress of Human Paleontology. Jaca Book: Milan. pp 387–390

    Google Scholar 

  62. 62.

    Manzi, G., et al (2010) The new chronology of the Ceprano calvarium (Italy). J Hum Evol 59(5):580–585

    PubMed  Article  Google Scholar 

  63. 63.

    Adam, K.D. (1985) The chronological and systematic position of the Steinheim skull. In: E. Delson, Editor Ancestors: The Hard Evidence. Alan R. Liss, Inc.: New York. pp 272–276

    Google Scholar 

  64. 64.

    Grün, R. (1996) A re-analysis of electron spin resonance dating results associated with the Petralona hominid. J Hum Evol 30 (3):227–241

    Article  Google Scholar 

  65. 65.

    Clark, J.D., et al (1994) African Homo erectus: old radiometric ages and young oldowan assemblages in the Middle Awash Valley, Ethiopia. Science 264:1907–1910

    CAS  PubMed  Article  Google Scholar 

  66. 66.

    Grün, R. and C. B. Stringer (1991) ESR dating and the evolution of modern humans. Archaeometry 33:153–99

    Article  Google Scholar 

  67. 67.

    Stringer, C. (2011) The chronological and evolutionary position of the Broken Hill cranium. Am J Phys Anthropol 144(S52):287

    Google Scholar 

  68. 68.

    Manega, P.C. (1995) New geochronological results from the Ndutu, Naisiusiu and Ngaloba Beds at Olduvai and Laetoli in northern Tanzania: their significance for evolution of modern humans. In Bellagio Conference. Italy

    Google Scholar 

  69. 69.

    Yin, G., et al (2001) Chronology of the stratum containing the skull of the Dali Man. Chinese Sci Bull 47(15):1302–1307

    Article  Google Scholar 

  70. 70.

    Chen, T., Q. Yang, and E. Wu (1994) Antiquity of Homo sapiens in China. Nature 368:55–60

    Article  Google Scholar 

  71. 71.

    Bruner, E. and G. Manzi (2006) Saccopastore 1: the earliest Neanderthal? A new look at an old cranium. In: K. Harvati and T. Harrison, Editors Neanderthals Revisited. Springer: New York. pp 23–36

    Google Scholar 

  72. 72.

    Oakley, K.P. (1964) The problem of man’s antiquity. An historical survey. Bull Br Mus Nat Hist 9(5):171–172

    Google Scholar 

  73. 73.

    Blackwell, B., et al (2007) ESR dating bovid teeth from the Neanderthal layer at La Ferrassie, France. Geol Soci Am 39(6):548

    Google Scholar 

  74. 74.

    Boule, M. (1911-1913) L’Homme fossile de La Chapelle-aux-Saints. Annls Paléont 6, 7, 8:109–172, 105-192, 1-62

    Google Scholar 

  75. 75.

    Bar-Yosef, O. (1998) Chronology of the Middle Paleolithic of the Levant. In: T. Akazawa, K. Aoki, and O. Bar-Yosef, Editors Neandertals and modern humans in Western Asia. Plenum: New York. pp 39–56

    Google Scholar 

  76. 76.

    Henry-Gambier, D. (2002) Les fossiles de Cro-Magnon (Les Eyzies-de-Tayac, Dordogne): nouvelles données sur leur position chronologique et leur attribution culturelle. Bull Mém Soc Anthrop Paris 14(1–2):89–112

    Google Scholar 

  77. 77.

    Bricker, H. and P. Mellars (1987) Datations 14C de l’Abri Pataud (Les Eyzies, Dordogne) par le procédé “accélérateur-spectromètre de masse”. L’Anthropologie 91:227–234

    Google Scholar 

  78. 78.

    Sonneville-Bordes, D. (1959) Position stratigraphique et chronologique relative des restes humains du Paléolithique Supérieur entre Loire et Pyrénées. Annls Paléont (Vert) 45:19–51

    Google Scholar 

  79. 79.

    Grün, R., et al (2005) U-series and ESR analyses of bones and teeth relating to the human burials from Skhul. J Hum Evol 49 (3):316–34

    PubMed  Article  Google Scholar 

  80. 80.

    Carmi, I. and D. Segal (1992) Rehovot radiocarbon measurements IV. Radiocarbon 34(1):115–132

    CAS  Google Scholar 

  81. 81.

    Swofford, D.L. (1993) Phylogenetic Analysis Using Parsimony (PAUP), Version 3.1.1. University of Illinois, Champaignp

    Google Scholar 

  82. 82.

    Maddison, D. R. and W. P. Maddison (2005) MacClade. Sunderland, Massachusetts: Sinauer Associates

    Google Scholar 

  83. 83.

    Wiley, E.O. (1981) Phylogenetics: The Theory and Practice of Phylogenetics Systematics. New York: John Wiley

    Google Scholar 

  84. 84.

    de Pinna, M.G.G. (1991) Concepts and Tests of Homology in the Cladistic Paradigm. Cladistics 7:367–394

    Article  Google Scholar 

  85. 85.

    Farris, J.S. (1989) The Retention Index and the Rescaled Consistency Index. Cladistics 5(4):417–419

    Article  Google Scholar 

  86. 86.

    Siebert, D.J. (1992) Tree statistics. In: T.S.A.P.N. 10, Editor Cladistics: A Practical Course in Systematics. Clarendon Press: Oxford. pp 72–88

    Google Scholar 

  87. 87.

    Sanderson, M. J. and M. J. Donoghue (1989) Patterns of Variation in Levels of Homoplasy. Evolution 43(8):1781–1795

    Article  Google Scholar 

  88. 88.

    Kauffman, S.A. (1993) The Origins of Order. Self-Organization and Selection in Evolution. New York: Oxford University Press

    Google Scholar 

  89. 89.

    Pope, G. (1992) Craniofacial evidence for the origin of modern humans in China. Yearb Phys Anthropol 35:243–98

    Article  Google Scholar 

  90. 90.

    Wu, X. and S. Athreya (2013) A description of the geological context, discrete traits, and linear morphometrics of the Middle Pleistocene hominin from Dali, Shaanxi Province, China. Am J Phys Anthropol 150(1):141–157

    PubMed  Article  Google Scholar 

  91. 91.

    Vandermeersch, B. (1981) Les Hommes de Qafzeh (Israël). Paris: CNRS. 319 p

    Google Scholar 

  92. 92.

    Hublin, J.-J. (1986) Some comments on the diagnostic features of Homo erectus. In: V. V. Novotny and A. Mizerova, Editors Fossil man. New facts - new ideas. Anthropos Institute - Moravian Museum: Brno. pp 175–187

    Google Scholar 

  93. 93.

    Condemi, S. (1988) Caractères plésiomorphes et apomorphes de l’os temporal des Néandertaliens européens würmiens. In: E. Trinkaus, Editor L’Anatomie. Université de Liège: Liège. pp 49–52

    Google Scholar 

  94. 94.

    Weidenreich, F. (1943) The skull of Sinanthropus pekinensis: A comparative study on a primitive hominid skull. Palaeontologia Sinica 10:1–485

    Google Scholar 

  95. 95.

    Maureille, B. (1994) La face chez Homo erectus et Homo sapiens: recherche sur la variabilité morphologique et métrique.Th èse de l’Université de Bordeaux 1. Anthropologie. pp. 634

    Google Scholar 

  96. 96.

    Rightmire, G.P. (1990) The Evolution of Homo erectus. Comparative Anatomical Studies of an Extinct Human Species. Vol. 1. Cambridge: Cambridge University Press. 260 p

    Google Scholar 

  97. 97.

    Orschiedt, J. (1996) Zur Frage der Manipulationen am Schädel des ” Homo steinheimensis “. In: I. Campen, J. Hahn, and M. Uerpmann, Editors Spuren der Jagd - Die Jagd nach Spuren. Festschrift Prof. Hansjürgen Müller-Beck. Tübinger Monographien zur Urgeschichte. MoVince: Tübingen. pp 467–472

    Google Scholar 

  98. 98.

    Rightmire, G.P., D. Lordkipanidze, and A. Vekua (2006) Anatomical descriptions, comparative studies and evolutionary significance of the hominin skulls from Dmanisi, Republic of Georgia. J Hum Evol 50(2):115–41

    PubMed  Article  Google Scholar 

  99. 99.

    Wu, R. (1988) The reconstruction of the fossil human skull from Jinniushan, Yinkoun Liaoning Province and its main features. Acta Anthropologica Sinica 7: 101–7

    Google Scholar 

  100. 100.

    Bräuer, G. (2008) The origin of modern anatomy: By speciation or intraspecific evolution? Evol Anthrop 17(1):22–37

    Article  Google Scholar 

  101. 101.

    Maddux, S. D. and R. G. Franciscus (2009) Allometric scaling of infraorbital surface topography in Homo. J Hum Evol 56 (2):161–174

    PubMed  Article  Google Scholar 

  102. 102.

    Freidline, S.E., et al (2012) A comprehensive morphometric analysis of the frontal and zygomatic bone of the Zuttiyeh fossil from Israel. J Hum Evol 62(2):225–241

    CAS  PubMed  Article  Google Scholar 

  103. 103.

    Rougier, H. and A. Balzeau (2007) La fosse sus-iniaque est-elle une autapomorphie des Néandertaliens? Analyse comparatives de ses caractéristiques morphologiques externes et internes. Bull Mém Soc Anthrop Paris 19:287

    Google Scholar 

  104. 104.

    Stringer, C.B. (2002) New perspectives on Neanderthals. Evol Anthrop Suppl 1:58–59

    Google Scholar 

  105. 105.

    Tattersall, I. and J. H. Schwartz (2006) The distinctiveness and systematic context of Homo neanderthalensis. In: K. Harvati and T. Harrison, Editors Neanderthals Revisited. Springer: New York. pp 9–22

    Google Scholar 

  106. 106.

    Arsuaga, J.L. (2010) Terrestrial apes and phylogenetic trees. P Natl Acad Sci USA 107:8910–8917

    CAS  Article  Google Scholar 

  107. 107.

    Bischoff, J.L., et al (2007) High-resolution U-series dates from the Sima de los Huesos hominids yields 600 ± 66 kyrs: implications for the evolution of the early Neanderthal lineage. JArchaeol Sci 34:763–770

    Article  Google Scholar 

  108. 108.

    Pérez, P.-J., et al (1997) Paleopathological evidence of the cranial remains from the Sima de los Huesos Middle Pleistocene site (Sierra de Atapuerca, Spain). Description and preliminary inferences. J Hum Evol 33:409–21

    PubMed  Article  Google Scholar 

  109. 109.

    Arsuaga, J.L., et al (2014) Neandertal roots: Cranial and chronological evidence from Sima de los Huesos. Science 344 (6190):1358–1363

    CAS  PubMed  Article  Google Scholar 

  110. 110.

    Fabre, V., S. Condemi, and A. Degioanni (2009) Genetic Evidence of Geographical Groups among Neanderthals. PLoS ONE 4(4):e5151

    PubMed Central  PubMed  Article  CAS  Google Scholar 

  111. 111.

    Condemi, S. (2001) Les Néanderthaliens de La Chaise. Documents préhistoire. Vol. 15. Paris: Comité des Travaux Historiques et Scientifiques. 178 p

    Google Scholar 

  112. 112.

    Condemi, S. (2007) Are there Neanderthals in the levant? In: M. Faerman, et al, Editors Faces from the Past -Diachronic Patterns in the Biology of Human Populations from the Eastern Mediterranean. BAR International Series 1603. Archaeopress: Oxford. pp 28–35

    Google Scholar 

  113. 113.

    Harvati, K., J.-J. Hublin, and P. Gunz (2010) Evolution of middlelate Pleistocene human cranio-facial form: A 3-D approach. J Hum Evol 59(5):445–464

    PubMed  Article  Google Scholar 

  114. 114.

    Trier, C.N., et al (2014) Evidence for Mito-Nuclear and Sex- Linked Reproductive Barriers between the Hybrid Italian Sparrow and Its Parent Species. PLoS Genet 10(1):e1004075

    PubMed Central  PubMed  Article  CAS  Google Scholar 

  115. 115.

    Holliday, T.W. (2003) Species Concepts, Reticulation, and Human Evolution. Curr Anthropol 44(5):653–673

    Article  Google Scholar 

  116. 116.

    Nelson, G. (1983) Reticulation in Cladograms. In: N. I. Platnick and V. A. Funk, Editors Advances in Cladistics: Proceedings and the Second Meeting of the Willi Hennig Society. Colombia University Press: New York. pp 105–114

    Google Scholar 

  117. 117.

    Wagner, W.H. (1983) Reticulistics: The recognition of hybrids and their role in cladistics and classification. In: N. I. Platnick and V. A. Funk, Editors Advances in Cladistics: Proceedings and the Second Meeting of the Willi Hennig Society. Colombia University Press: New York. pp 63–79

    Google Scholar 

  118. 118.

    Pardi, F. and C. Scornavacca (2015) Reconstructible Phylogenetic Networks: Do Not Distinguish the Indistinguishable. PLoS Comput Biol 11(4):e1004135

    PubMed Central  PubMed  Article  Google Scholar 

  119. 119.

    Wanntorp, H.E. (1983) Reticulated cladograms and the identification of hybrid taxa. In: N. I. Platnick and V. A. Funk, Editors Advances in Cladistics: Proceedings and the Second Meeting of the Willi Hennig Society. Colombia University Press: New York. pp 81–88

    Google Scholar 

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Mounier, A., Caparros, M. The phylogenetic status of Homo heidelbergensis – a cladistic study of Middle Pleistocene hominins. BMSAP 27, 110–134 (2015). https://doi.org/10.1007/s13219-015-0127-4

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Keywords

  • Homo heidelbergensis
  • Cladistics
  • Last common ancestor of modern humans and Neandertals
  • Sima de los Huesos

Mots clés

  • Homo heidelbergensis
  • Cladistique
  • Dernier ancêtre commun des Hommes modernes et des Néandertaliens
  • Sima de los Huesos