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Neanderthals and modern humans: an example of a mammalian syngameon?

  • T. W. Holliday
Part of the Vertebrate Paleobiology and Paleoanthropology book series (VERT)

Lotsy (1925) suggested that hybridizing plant species be grouped into larger interbreeding taxa that he named “syngameons.” Such hybridizing taxa have long been well-documented among plants, but zoologists have traditionally downplayed the role of hybridization in animal evolution. Templeton (1989), however, has recently suggested that mammalian species which freely hybridize should also be grouped into syngameons. A literature survey suggests that the ability of any two mammalian species to hybridize successfully (i.e., produce viable, fertile hybrid offspring) is negatively correlated with time since phylogenetic divergence. In this regard, the genus Homo is a prime candidate for the presence of syngameons since the genus Homo (sensu stricto Wood and Collard, 1999) only emerged ca. 2.0 million years ago. The Late Pleistocene paleospecies Homo neanderthalensis is morphologically quite distinct from H. sapiens. The marked morphological (and genetic) distance between these two members of the genus Homo has led many human paleontologists to infer that these two taxa are separate species. From a current systematic perspective, such a position is justified, since in almost all species concepts species are defined by characters, of which the ability to interbreed is only one. In fact, the ability to interbreed is a plesiomorphic character, and as such we should not be surprised if two sister taxa, such as H. neanderthalensis and H. sapiens, retain this ability. There is, however, a relative dearth of paleontological evidence for such interbreeding — a somewhat surprising finding that warrants further exploration.

Keywords

hybridization species concepts modern human origins divergence times 

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References

  1. Adcock, G., Dennis, E., Easteal, S., Huttley, G., Jermin, L., Peacock, W., Thorne, A., 2001. Mitochondrial DNA sequences in ancient Australians: Implications for modern human origins. Proc. Natl. Acad. Sci. U.S.A. 98, 537–542.CrossRefGoogle Scholar
  2. Ballinger, S.W., Blankenship, L.H., Bickham, J.W., Carr, S.M., 1992. Allozyme and mitochondrial DNA analysis of a hybrid zone between whitetailed deer and mule deer (Odocoileus) in west Texas. Biochem. Genet. 30, 1–11.CrossRefGoogle Scholar
  3. Barton, N.H., 2001. The role of hybridization in evolution. Mol. Ecol. 10, 551–568.CrossRefGoogle Scholar
  4. Bermúdez de Castro, J.M., Arsuaga, J.L., Carbonell, E., Rosas, A., Martínez, I., Mosquera, M., 1997. A hominid from the Lower Pleistocene of Atapuerca, Spain: Possible ancestor to Neandertals and modern humans. Science 276, 1392–1395.CrossRefGoogle Scholar
  5. Bininda-Emonds, O.R.P., Gittleman, J.L., Purvis, A., 1999. Building large trees by combining phylogenetic information: a complete phylogeny of the extant Carnivora (Mammalia). Biol. Rev. 74, 143–175.CrossRefGoogle Scholar
  6. Brashares, J.S., Garland, T., Jr., Arcese, P., 2000. Phylogenetic analysis of coadaptation in behavior, diet, and body size in the African antelope. Behav. Ecol. 11, 452–463.CrossRefGoogle Scholar
  7. Bräuer, G., 1992. Africa’s place in the evolution of Homo sapiens. In: Bräuer, G., Smith, F.H. (Eds.), Continuity or Replacement: Controversies in Homo sapiens Evolution. A. A. Balkema, Rotterdam, pp. 83–98.Google Scholar
  8. Brownlow, C.A., 1996. Molecular taxonomy and the conservation of the red wolf and other endangered carnivores. Conserv. Biol. 10, 390–396.CrossRefGoogle Scholar
  9. Caramelli, D., Lalueza-fox, C., Vernesi, C., Lari, M., Casoli, A., Mallegni, F., Chiarelli, B., Dupanloup, I., Bertranpetit, J., Barbujani, G., Bertorelle, G. 2003. Evidence for a genetic discontinuity between Neandertals and 24,000- year-old anatomically modern Europeans. Proc. Natl. Acad. Sci. U.S.A. 100, 6593–6597.CrossRefGoogle Scholar
  10. Cathey, J.C., Bickham, J.W., Patton, J.C., 1998. Introgressive hybridization and nonconcordant evolutionary history of maternal and paternal lineages in North American deer. Evolution 52, 1224–1229.CrossRefGoogle Scholar
  11. Churchill, S.E., 1996. Particulate versus integrated evolution of the upper body in Late Pleistocene humans: A test of two models. Am. J. Phys. Anthropol. 100, 559–583.CrossRefGoogle Scholar
  12. Churchill, S.E., Smith, F.H., 2000. Makers of the Early Aurignacian of Europe. Yrbk. Phys. Anthropol. 43, 61–115.CrossRefGoogle Scholar
  13. Cracraft, J., 1983. Species concepts and speciation analysis. Curr. Ornithol. 1, 159–187.CrossRefGoogle Scholar
  14. Cracraft, J., 1989. Speciation and its ontology: the empirical consequences of alternative species concepts for understanding patterns and processes of differentiation. In: Otte, D., Endler, J.A. (Eds.), Speciation and its Consequences. Sinauer Associates, Sunderland, MA, pp. 28–59.Google Scholar
  15. d’Errico, F., Soressi, M., 2002. Systematic use of manganese pigment by the Pech-de-l’Azé Neandertals: Implications for the origin of behavioral modernity. J. Hum. Evol. 42, A13.Google Scholar
  16. d’Errico, F., Zilhão, J., Baffier, D., Julien, M., Pelegrin, J., 1998. Neandertal acculturation in Western Europe? A critical review of the evidence and its interpretation. Curr. Anthropol. 39, 1–44.CrossRefGoogle Scholar
  17. De Queiroz, K., 1998. The general lineage concept of species, species criteria, and the process of speciation: A conceptual unification and terminological recommendations. In: Howard, D.J., Berlocher, S.H. (Eds.), Endless Forms: Species and Speciation. Oxford University Press, Oxford, pp. 57–75.Google Scholar
  18. Duarte, C., Mauricio, J., Pettitt, P.B., Souto, P., Trinkaus, E., van der Plicht, H., Zilhão, J., 1999. The early Upper Paleolithic human skeleton from the Abrigo do Lagar Velho (Portugal) and modern human emergence in Iberia. Proc. Natl. Acad. Sci. U.S.A. 96, 7604–7609.CrossRefGoogle Scholar
  19. Franciscus, R.G., 1996. Neandertal nasal structures and upper respiratory tract “specialization.” Proc. Natl. Acad. Sci. U.S.A. 96, 1805–1809.CrossRefGoogle Scholar
  20. Franciscus, R.G., Schoenebaum, C.R., 2000. Crosssectional metric analysis of scapular axillary border morphology in recent humans and the Krapina Neandertals. Am. J. Phys. Anthropol. (Suppl. 30), 152.Google Scholar
  21. Frayer, D.W., 1992. Evolution at the European edge: Neanderthal and Upper Paleolithic relationships. Préhist. Europ. 2, 9–69.Google Scholar
  22. Frayer, D.W., Wolpoff, M.H., Thorne, A.G., Smith, F.H., Pope, G.G., 1993. Theories of modern human origins: The paleontological test. Am. Anthropol. 95, 14–50.CrossRefGoogle Scholar
  23. Gray, A., 1972. Mammalian Hybrids. A Check-list with Bibliography. 2nd Edition. Commonwealth Agricultural Bureaux, Farnham Royal, Buckinghamshire, UK.Google Scholar
  24. Haldane, J.B.S., 1922. Sex ratio and unisexual sterility of hybrid animals. J. Genet. 12, 101–109.CrossRefGoogle Scholar
  25. Hall, R.L., 1978. Variability and speciation in canids and hominids. In: Hall, R.L., Sharp, H.S. (Eds.), Wolf and Man: Evolution in Parallel. Academic Press, New York, pp. 153–177.Google Scholar
  26. Harvati, K., 2003. The Neanderthal taxonomic position: Models of intra- and inter-specific craniofacial variation. J. Hum. Evol. 44, 107–132.CrossRefGoogle Scholar
  27. Harvati, K., Frost, S.R., McNulty, K.P., 2004. Neanderthal taxonomy reconsidered: implications of 3D primate models of intra- and interspecific differences. Proc. Natl. Acad Sci. U.S.A. 101, 1147–1152.CrossRefGoogle Scholar
  28. Hawks, J., Wolpoff, M.H., 2001. Paleoanthropology and the population genetics of ancient genes. Am. J. Phys. Anthropol. 114, 269–272.CrossRefGoogle Scholar
  29. Henshilwood, C.S., Marean, C.W., 2003. The origin of modern human behaviour: a review and critique of models and test implications. Curr. Anthropol. 44, 627–651.CrossRefGoogle Scholar
  30. Hilton, H., 1978. Systematics and ecology of the eastern coyote. In: Bekoff, M. (Ed.), Coyotes: Biology, Behavior, and Management. Academic Press, New York, pp. 209–228.Google Scholar
  31. Holliday, T.W., 1997. Body proportions in Late Pleistocene Europe and modern human origins. J. Hum. Evol. 32, 423–448.CrossRefGoogle Scholar
  32. Holliday, T.W., 2000. Evolution at the crossroads: Modern human emergence in Western Asia. Am. Anthropol. 102, 54–68.CrossRefGoogle Scholar
  33. Holliday, T.W., 2003. Species concepts, reticulation, and human evolution. Curr. Anthropol. 44, 653–673.CrossRefGoogle Scholar
  34. Holloway, R.L., 1985. The poor brain of Homo sapiens neanderthalensis: See what you please. In: Delson, E. (Ed.), Ancestors: The Hard Evidence. Alan R. Liss, New York, pp. 319–324.Google Scholar
  35. Howell, F.C., 1994.A chronostratigraphic and taxonomic framework of the origins of modern humans. In: Nitecki, M.H., Nitecki D.V. (Eds.), Origins of Anatomically Modern Humans. Plenum Press, NewYork, pp. 253–319.CrossRefGoogle Scholar
  36. Hublin, J.-J., 1998. Climatic changes, paleogeography, and the evolution of the Neandertals. In Akazawa, T., Aoki, K., Bar-Yosef, O. (Eds.), Neandertals and Modern Humans in Western Asia. Plenum Press, New York, pp. 295–310.Google Scholar
  37. Jablonski, N.G., 2004. The Evolution of human skin and skin color. Ann. Rev. Anthropol. 33, 585–623.CrossRefGoogle Scholar
  38. Jolly, C.J., 2001. A proper study for mankind: Analogies from papionin monkeys and their implications for human evolution. Yrbk. Phys. Anthropol. 44, 177–204.CrossRefGoogle Scholar
  39. Jolly, C.J., Woolley-Barker, T., Beyene, S., Disotell, T.R., Phillips-Conroy, J.E., 1997. Intergeneric hybrid baboons. Int. J. Primatol. 18, 597–627.CrossRefGoogle Scholar
  40. Kappelman, J., 1996. The evolution of body mass and relative brain size in fossil hominids. J. Hum. Evol. 30, 243–276.CrossRefGoogle Scholar
  41. King, W., 1864. The reputed fossil man of the Neanderthal. Quart. Rev. Sci., 1, 88–97.Google Scholar
  42. Klein, R.G., 2003. Whither the Neanderthals? Science 299, 1525–1527.CrossRefGoogle Scholar
  43. Krings, M., Stone, A., Schmitz, R.W., Krainitzki, H., Stoneking, M., Pääbo, S. 1997. Neandertal DNA sequences and the origin of modern humans. Cell 90, 19–30.CrossRefGoogle Scholar
  44. Krings, M., Capelli, C., Tschentscher, F., Geisert, H., von Haiseler Meyer, S., Grossschmidt, A., Possnert, G., Paunovic, M., Pääbo, S. 2000. A view of Neandertal genetic diversity. Nat. Genet. 26, 144–46.CrossRefGoogle Scholar
  45. Lahr, M.M., Foley, R., 1998. Towards a theory of modern human origins: Geography, demography, and diversity in recent human evolution. Yrbk. Phys. Anthropol. 41, 137–176.CrossRefGoogle Scholar
  46. Lehman, N., Eisenhawer, A., Hansen, K., Mech, L.D., Peterson, R.O., Gogan, P.J.P., Wayne, R.K., 1991. Introgression of coyote mitochondrial DNA into sympatric North American gray wolf populations. Evolution 45, 104–119.CrossRefGoogle Scholar
  47. Lotsy, J.P., 1925. Species or linneon. Genetica 7, 487–506.CrossRefGoogle Scholar
  48. MacFadden, B.J., 1992. Fossil Horses: Systematics, Paleobiology, and Evolution of the Family Equidae. Cambridge University Press, New York.Google Scholar
  49. Mayden, R.L., 1997. The hierarchy of species concepts: The denouement in the saga of the species problem. In: Claridge, M.A., Dawah, H.A., Wilson, M.R. (Eds.), Species: The Units of Biodiversity. Chapman and Hall, New York, pp. 381–424.Google Scholar
  50. Mayr, E., 1942. Systematics and the Origin of Species from the Viewpoint of a Zoologist. Columbia University Press, New York.Google Scholar
  51. Mayr, E., 1963. Animal Species and Evolution. Belknap Press, Cambridge, MA.Google Scholar
  52. Mayr, E., 2000. The biological species concept. In: Wheeler, Q.D., Meier, R. (Eds.), Species Concepts and Phylogenetic Theory: A Debate. Columbia University Press, New York, pp. 17–29.Google Scholar
  53. Meijaard, E., Groves, C.P., 2004. Morphometrical relationships between south-east Asian deer (Cervidae, Tribe Cervini): evolutionary and biogeographic implications. J. Zool., Lond. 263, 179–196.CrossRefGoogle Scholar
  54. Mellars, P., 2005. The impossible coincidence. A singlespecies model for the origins of modern human behavior in Europe. Evol. Anthrop. 14, 12–27.CrossRefGoogle Scholar
  55. Mishler, B.D., Theriot, E.C., 2000. The phylogenetic species concept (sensu Mishler and Theriot): Monophyly, apomorphy, and phylogenetic species concepts. In: Wheeler, Q.D., Meier, R. (Eds.), Species Concepts and Phylogenetic Theory: A Debate. Columbia University Press, New York, pp. 44–54.Google Scholar
  56. Nowak, R.M., 1978. Evolution and taxonomy of coyotes and related Canis. In: Bekoff, M. (Ed.), Coyotes: Biology, Behavior, and Management. Academic Press, New York, pp. 3–16.Google Scholar
  57. Oakenfull, E.A., Clegg, J.B., 1998. Phylogenetic relationships within the genus Equus and the evolution of α and θ globin genes. J. Mol. Evol. 47, 772–783.CrossRefGoogle Scholar
  58. Oakenfull, E.A., Lim, H.N., Ryder, O.A., 2000. A survey of equid mitochondrial DNA: Implications for the evolution, genetic diversity and conservation of Equus. Conserv. Genet. 1, 341–355.CrossRefGoogle Scholar
  59. Ovchinnikov, I.V., Götherström, A, Romanova, G.P., Kharitonov, V.M., Lindén, K., Goodwin, W., 2000. Molecular analysis of Neanderthal DNA from the northern Caucasus. Nature 404, 490–493.CrossRefGoogle Scholar
  60. Pitra, C., Fickel, J., Meijaard, E., Groves, P.C., 2004. Evolution and phylogeny of Old World deer. Mol. Phylogen. Evol. 33, 880–895.CrossRefGoogle Scholar
  61. Purvis, A., Bromham, L., 1997. Estimating the transition/ transversion ratio from independent pairwise comparisons with an assumed phylogeny. J. Mol. Evol. 44, 112–119.CrossRefGoogle Scholar
  62. Rak, Y., 1986. The Neanderthal: A new look at an old face. J. Hum. Evol. 15, 151–164.CrossRefGoogle Scholar
  63. Rak, Y., 1998. Does any Mousterian cave present evidence of two hominid species? In Akazawa, T., Aoki, K., Bar-Yosef, O. (Eds.), Neandertals and Modern Humans in Western Asia. Plenum Press, New York, pp. 353–366.Google Scholar
  64. Relethford, J.H., 1995. Genetics and modern human origins. Evol. Anthropol. 4, 53–63.CrossRefGoogle Scholar
  65. Relethford, J.H., 1998. Genetics of modern human origins and diversity. Ann. Rev. Anthropol. 27, 1–23.CrossRefGoogle Scholar
  66. Relethford, J.H., Harpending, H.C., 1995. Ancient differences in population size can mimic a recent African origin of modern humans. Curr. Anthropol. 36, 667–674.CrossRefGoogle Scholar
  67. Ritz, L.R., Glowatzki-Mullis, M.-L., MacHugh, D.E., Gaillard, C., 2000. Phylogenetic analysis of the Tribe Bovini using microsatellites. Animal Genet. 31, 178–185.CrossRefGoogle Scholar
  68. Roy, M.S., Girman, D.J., Taylor, A.C., Wayne, R.K., 1994. The use of museum specimens to reconstruct genetic variability and relationships of extinct populations. Experientia 50, 551–557.CrossRefGoogle Scholar
  69. Ruff, C.B., Trinkaus, E., Holliday, T.W., 1997. Body mass and encephalization in Pleistocene Homo. Nature 387, 173–176.CrossRefGoogle Scholar
  70. Schillaci, M.A., Froehlich, J.W., 2001. Nonhuman primate hybridization and the taxonomic status of Neanderthals. Am. J. Phys. Anthropol. 115, 157–166.CrossRefGoogle Scholar
  71. Schwartz, M.K., Pilgrim, K.L., McKelvey, K.S., Lindquist, E.L., Claar, J.J., Loch, S., Ruggiero, L.F., 2004. Hybridization between Canada lynx and bobcats: Genetic results and management implications. Conserv. Genet. 5, 349–355.CrossRefGoogle Scholar
  72. Serre, D., Langaney, A., Chech, M., Teschler-Nicola, M., Paunovic, M., Mennecier, P., Hofreiter, M., Possnert, G., Paabo, S., 2004. No evidence of Neandertal mtDNA contribution to early modern humans. PLoS Biol. 2, 313–317.CrossRefGoogle Scholar
  73. Shea, J.J., 2003. Neandertals, competition, and the origin of modern human behavior in the Levant. Evol. Anthropol. 12, 173–187.CrossRefGoogle Scholar
  74. Shreeve, J., 1995. The Neandertal Enigma: Solving the Mystery of Modern Human Origins. William Morrow, New York.Google Scholar
  75. Simpson, G.G., 1961. Principles of Animal Taxonomy. Columbia University Press, New York.Google Scholar
  76. Skinner, A.R., Blackwell, B.A.B., Martin, S., Ortega, A., Blickstein, J.I.B., Golovanova, L.V., Doronichev, V.B. 2005. ESR dating at Mezmaiskaya Cave, Russia. Appl. Radiat. Isot. 62, 219–224.CrossRefGoogle Scholar
  77. Smith, F.H., 1984. Fossil hominids from the Upper Pleistocene of Central Europe and the origin of modern Europeans. In: Smith, F.H., Spencer, F. (Eds.), The Origins of Modern Humans: A World Survey of the Fossil Evidence. Alan R. Liss, New York, pp. 137–209.Google Scholar
  78. Smith, F.H., 1985. Continuity and change in the origin of modern Homo sapiens. Z. Morph. Anthrop. 75, 197–222.Google Scholar
  79. Smith, F.H., 1992. The role of continuity in modern human origins. In: Bräuer, G., Smith, F.H. (Eds.), Continuity or Replacement: Controversies in Homo sapiens Evolution. Balkema, Rotterdam, pp. 145–156.Google Scholar
  80. Stringer, C., 2002. Modern human origins: Progress and prospects. Phil. Trans. R. Soc. Lond. B 357, 563–579.CrossRefGoogle Scholar
  81. Stringer, C.B., Andrews, P., 1988. Genetic and fossil evidence for the origin of modern humans. Science 239, 1263–1268.CrossRefGoogle Scholar
  82. Tattersall, I., 1992. Species concepts and species identification in human evolution. J. Hum. Evol. 22, 341–349.CrossRefGoogle Scholar
  83. Tattersall, I., 1999. The Last Neanderthal: The Rise, Success, and Mysterious Extinction of our Closest Human Relatives. Revised Edition. Westview Press, Boulder, CO.Google Scholar
  84. Templeton, A.R., 1989. The meaning of species and speciation: A genetic perspective. In: Otte, D., Endler, J.A. (Eds.), Speciation and its Consequences. Sinauer Associates, Sunderland, MA, pp. 3–27.Google Scholar
  85. Trinkaus, E., 1987. The Neandertal face: Evolutionary and functional perspectives on a recent hominid face. J. Hum. Evol. 16, 429–443.CrossRefGoogle Scholar
  86. Trinkaus, E., 1995. Near Eastern late archaic humans. Paléorient 21, 9–23.CrossRefGoogle Scholar
  87. Trinkaus, E., Zilhão, J., 2002. Phylogenetic implications of Lagar Velho 1. In: Zilhão, J., Trinkaus, E. (Eds.), Portrait of the Artist as a Child: The Gravettian Human Skeleton from the Abrigo do Lagar Velho and Its Archeological Context. Instituto Português de Arqueologia, Lisbon, Trabalhos de Arqueologia 22, pp. 497–518.Google Scholar
  88. Vilà, C., Leonard, J.A., Götherström, A., Marklund, S., Sandberg, K., Lidén, K., Wayne, R.K., Ellegren, H., 2001. Widespread origins of domestic horse lineages. Science 291, 474–477.CrossRefGoogle Scholar
  89. Wayne, R.K., Jenks, S.M., 1991. Mitochondrial DNA analysis implying extensive hybridization of the endangered red wolf Canis rufus. Nature 351, 565–568.CrossRefGoogle Scholar
  90. Wayne, R.K., Van Valkenburgh, B., O’Brien S.J., 1991. Molecular distance and divergence time in carnivores and primates. Mol. Biol. Evol. 8, 297–319.Google Scholar
  91. Wayne, R.K., Lehman, N., Allard, M.W., Honeycutt, R.L., 1992. Mitochondrial DNA variability of the gray wolf: Genetic consequences of population decline and habitat fragmentation. Conserv. Biol. 6, 559–569.CrossRefGoogle Scholar
  92. White, M.J.D., 1973. Animal Cytology and Evolution. 3rd Edition. Cambridge University Press, Cambridge.Google Scholar
  93. Wiley, E.O., 1981. Phylogenetics: The Theory and Practice of Phylogenetic Systematics. Wiley, New York.Google Scholar
  94. Wiley, E.O., Mayden, R.L., 2000. The evolutionary species concept. In: Wheeler, Q.D., Meier, R. (Eds.), Species Concepts and Phylogenetic Theory: A Debate. Columbia University Press, New York, pp. 70–89.Google Scholar
  95. Wood, B., Collard, M., 1999. The human genus. Science 284, 65–71.Google Scholar
  96. Wood, B., Richmond, B.G., 2000. Human evolution: Taxonomy and paleobiology. J. Anat. 196, 19–60.CrossRefGoogle Scholar
  97. Wolpoff, M.H., 1999. Paleoanthropology. 2nd Edition. McGraw-Hill, Boston.Google Scholar
  98. Wolpoff, M.H., 2003. Comment to Holliday. Curr. Anthropol. 44, 666–667.Google Scholar
  99. Xu, X. Gullberg, A., Arnason, U., 1996. The complete mitochondrial DNA (mtDNA) of the donkey and mtDNA comparisons among four closely related mammalian species-pairs. J. Mol. Evol. 43, 438–444.CrossRefGoogle Scholar
  100. Zeh, D.W., Zeh, J.A., 2000. Reproductive mode and speciation: the viviparity-driven conflict hypothesis. BioEssays 22, 938–946.CrossRefGoogle Scholar

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© Springer 2006

Authors and Affiliations

  • T. W. Holliday
    • 1
  1. 1.Department of AnthropologyTulane UniversityNew OrleansUSA

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