International Journal of Primatology

, Volume 30, Issue 5, pp 643–662 | Cite as

Reappraisal of Macaca speciosa subfossilis from the Late Pleistocene of Northern Vietnam Based on the Analysis of Cranial Anatomy

  • Tsuyoshi Ito
  • Takeshi D. Nishimura
  • Brigitte Senut
  • Thomas Koppe
  • Jacque Treil
  • Masanaru Takai
Article

Abstract

Jouffroy (Bulletin du Muséum National d'Histoire Naturelle. Série 2 31:209–216, 1959) described Macaca speciosa subfossilis on the basis of her study of the external anatomy of a nearly complete cranium (PV F1; Muséum national d’Histoire naturelle, Paris) found in the Late Pleistocene cave deposits, Thung-Lang, northern Vietnam. Whereas Jouffroy (Bulletin du Muséum National d'Histoire Naturelle. Série 2 31:209–216, 1959) considered it to belong to an ancestor of Macaca arctoides or M. thibetana, Fooden (Journal of Human Evolution 19:607–686, 1990) reexamined the facial anatomy and assigned it to the extant species M. arctoides. We used computed tomography images to reevaluate the phylogenetic position of Macaca speciosa subfossilis by comparing the external and internal features of PV F1 with those of the crania of the extant macaque species. PV F1 shows a lower degree of preorbital concavity than Macaca arctoides, M. assamensis, and M. thibetana, but shares an anteriorly directed malar as seen in the crania of the two former species. The size of the molars of PV F1 falls within a range such that the cranium may be assigned to any of the five species of Macaca arctoides, M. assamensis, M. thibetana, M. mulatta, and M. nemestrina. An analysis of the internal structure of the cranium reveals that only PV F1 and the cranium of Macaca arctoides have a pear-shaped nasal cavity expanding laterally at both the anterior and posterior regions. Such a feature is probably a derived condition in the macaque lineage, suggesting a close relationship between Macaca speciosa subfossilis and M. arctoides. This finding supports the paleobiological scenario that the members of the lineage of Macaca arctoides diverged from the other members of Asian macaques and became distributed in northern Vietnam as early as the Late Pleistocene.

Keywords

computed tomography macaque maxillary sinus nasal cavity 

Notes

Acknowledgments

We thank the Muséum national d’Histoire naturelle (Paris), the Japan Monkey Centre (JMC), Okayama University Hospital, and Laboratory of Physical Anthropology (KAS) and the Primate Research Institute (PRI) of the Kyoto University for offering us the opportunities to scan the specimens. We thank Todd C. Rae of the University of Roehampton; Daisuke Shimizu of JMC; José Braga in the Université Paul Sabatier; Arnaud Beck in the Institut de Médecine et de Physiologie Spatiales; Sylvie Charreau and Albeal Mvoto of the Clinique Pasteur, Toulouse; Masato Nakatsukasa, Naomichi Ogihara, and Wataru Yano of KAS; Zin Maung Maung Thein of PRI; and Taung Htike of Shwebo Degree College for their help for CT scanning. We thank Naoko Egi of PRI for her supportive advice on phyletic analysis, and Elizabeth Nakajima for checking the English text. We also greatly appreciate Joanna Setchell and 2 anonymous reviewers for improving the quality of this paper. This research was financially supported in part by a Grant-in-Aid for Scientific Research from the Japan Society for the Promotion of Science Grant 21770263 to T. D. Nishimura; Grant 20405015 to M. Takai), by the Ito Foundation, Tokyo (to T. D. Nishimura), by GDRI CNRS, France (to B. Senut), and by the Global Center of Excellence Program Formation of a Strategic Base for Biodiversity and Evolutionary Research: from Genome to Ecosystem of the Ministry of Education, Culture, Sports, Science and Technology, Japan (Grant A06 to Kyoto University).

References

  1. Cronin, J. E., Cann, R., & Sarich, V. M. (1980). Molecular evolution and systematics of the genus Macaca. In D. G. Lindburg (Ed.), The macaques: Studies in ecology, behavior and evolution (pp. 31–51). New York: Van Nostrand Reinhol.Google Scholar
  2. Deinard, A., & Smith, D. G. (2001). Phylogenetic relationships among the macaques: evidence from the nuclear locus NRAMP1. Journal of Human Evolution, 41, 45–59.PubMedCrossRefGoogle Scholar
  3. Delson, E. (1980). Fossil Macaques, phyletic relationships and a scenario of deployment. In D. G. Lindburg (Ed.), The macaques: Studies in ecology, behavior and evolution (pp. 10–30). New York: Van Nostrand Reinhol.Google Scholar
  4. Farris, J. S. (1989). The retention index and the rescaled consistency index. Cladistics, 5, 417–419.CrossRefGoogle Scholar
  5. Fooden, J. (1980). Classification and distribution of living macaques (Macaca Lacépède, 1799). In D. G. Lindburg (Ed.), The macaques: Studies in ecology, behavior and evolution (pp. 1–9). New York: Van Nostrand Reinhol.Google Scholar
  6. Fooden, J. (1988). Taxonomy and evolution of the sinica group of macaques: 6. Interspecific comparisons and synthesis. Fieldiana Zool, 45, 1–44.Google Scholar
  7. Fooden, J. (1990). The bear macaques, Macaca arctoides: a systematic review. Journal of Human Evolution, 19, 607–686.CrossRefGoogle Scholar
  8. Fooden, J., & Lanyon, S. M. (1989). Blood-protein allele frequencies and phylogenetic relationships in macaca: a review. American Journal of Primatology, 17, 209–241.CrossRefGoogle Scholar
  9. Jablonski, N. G. (2002). Fossil old world monkeys: The late Neogene radiation. In W. C. Hartwig (Ed.), The primate fossil record (pp. 255–299). New York: Cambridge University Press.Google Scholar
  10. Jouffroy, F. K. (1959). Un crane subfossile de macaque du Pléistocène du Viet Nam. Bulletin du Muséum National d’Histoire Naturelle. Série 2, 31, 209–216.Google Scholar
  11. Koppe, T., & Nagai, T. (1999). Quantitative analysis of the maxillary sinus in Catarrhine Primates. In T. Koppe, H. Nagai & K. W. Alt (Eds.), The paranasal sinuses of highter primates: development, function, and evolution (p. 121). Berlin: Quintessence.Google Scholar
  12. Koppe, T., & Ohkawa, Y. (1999). Pneumatization of the facial skelton in Catarrhine Primates. In T. Koppe, H. Nagai & K. W. Alt (Eds.), The paranasal sinuses of highter primates: development, function, and evolution (pp. 77–119). Berlin: Quintessence.Google Scholar
  13. Koppe, T., & Rae, T. C. (2001). Factors influencing the pneumatization of the alveolar process in Macaques. In A. Brook (Ed.) 12th International symposium on dental morphology (pp. 267–276). Sheffield: Sheffield Academic Press Ltd.Google Scholar
  14. Koppe, T., Rae, T. C., & Swindler, D. R. (1999). Influence of craniofacial morphology on primate paranasal pneumatization. Annals of Anatomy, 181, 77–80.PubMedCrossRefGoogle Scholar
  15. Li, Q. Q., & Zhang, Y. P. (2005). Phylogenetic relationships of the macaques (Cercopithecidae: Macaca), inferred from mitochondrial DNA sequences. Biochemical Genetics, 43, 375–386.PubMedCrossRefGoogle Scholar
  16. Liu, D., & Ding, M. (1984). The characteristics and evolution of the palaeoenvironment of China since the Late Tertiary. In R. O. Whyte (Ed.) The Evolution of the East Asian environment (pp. 11-40) Hong Kong: Center of Asian studies, University of Hong Kong.Google Scholar
  17. Maddison, D. R., & Maddison, W. P. (2000). MacClade 4: Analysis of phylogeny and character evolution. Version 4.0. Sunderland: Sinauer Associates.Google Scholar
  18. Morales, J. C., & Melnick, D. J. (1998). Phylogenetic relationships of the macaques (Cercopithecidae: Macaca), as revealed by high resolution restriction site mapping of mitochondrial ribosomal genes. Journal of Human Evolution, 34, 1–23.PubMedCrossRefGoogle Scholar
  19. Nishimura, T. D., Takai, M., & Maschenko, E. N. (2007). The maxillary sinus of Paradolichopithecus sushkini (late Pliocene, southern Tajikistan) and its phyletic implications. Journal of Human Evolution, 52, 637–646.PubMedCrossRefGoogle Scholar
  20. Pan, R., Jablonski, N. G., Oxnard, C., & Freedman, L. (1998). Morphometric analysis of Macaca arctoides and M. thibetana in relation to other macaque species. Primates, 39, 519–537.CrossRefGoogle Scholar
  21. Rae, T. C. (2008). Paranasal pneumatization in extant and fossil Cercopithecoidea. Journal of Human Evolution, 54, 279–286.PubMedCrossRefGoogle Scholar
  22. Rae, T. C., Hill, R. A., Hamada, Y., & Koppe, T. (2003). Clinical variation of sinus volume in Japanese Macaques (Macaca fuscata). American Journal of Primatology, 59, 153–158.PubMedCrossRefGoogle Scholar
  23. Rae, T. C., Röhrer–Ertl, O., Wallner, C–. P., & Koppe, T. (2007). Paranasal pneumatization of two late Miocene colobines: Mesopithecus and Libypithecus (Cercopithecidae: Primates). Journal of Vertebrate Paleontology, 27, 768–771.CrossRefGoogle Scholar
  24. Rossie, J. B. (2005). Anatomy of the nasal cavity and paranasal sinuses in Aegyptopithecus and early Miocene African Catarrhines. American Journal of Anthropology, 126, 250–267.CrossRefGoogle Scholar
  25. Rossie, J. B., Simons, E. L., Gauld, S. C., & Rasmussen, D. T. (2002). Paranasal sinus anatomy of Aegyptopithecus: implications for hominoid origins. Proceedings of the National Academy of Sciences, 99, 8454–8456.CrossRefGoogle Scholar
  26. Schlosser, M. (1924). Fossil Primates from China. Palaeontologia Sinica. Series C, 1, 1–16.Google Scholar
  27. Singleton, M. (2002). Patterns of cranial shape variation in the Papionini (Primates; Cercopithecinae). Journal of Human Evolution, 42, 547–578.PubMedCrossRefGoogle Scholar
  28. Smith, T. D., Rossie, J. B., & Bhatnagar, K. P. (2007). Evolution of the nose and nasal skeleton in Primates. Evolutionary Anthropology, 16, 132–146.CrossRefGoogle Scholar
  29. Stierna, P. L. E. (2001). Physiology, mucociliary clearance, and neural control. In D. Kennedy, W. Bolger & S. Zinnreich (Eds.), Diseases of the sinuses: Diagnosis and management (pp. 35–45). Hamilton: B.C. Decker.Google Scholar
  30. Szalay, F. S., & Delson, E. (1979). Evolutionary history of the primates. New York: Academic.Google Scholar
  31. Thierry, B., Iwaniuk, A. N., & Pellis, S. M. (2000). The influence of phylogeny on the social behavior of macaques (Primates: Cercopithecidae, genus Macaca). Ethology, 106, 713–728.CrossRefGoogle Scholar
  32. Tosi, A. J., Morales, J. C., & Melnick, D. J. (2000). Comparison of Y chromosome and mtDNA phylogenies leads to unique inferences of macaque evolutionary history. Molecular Phylogenetics and Evolution, 17, 133–144.PubMedCrossRefGoogle Scholar
  33. Tosi, A. J., Morales, J. C., & Melnick, D. J. (2003). Paternal, maternal, and biparental molecular markers provide unique windows onto the evolutionary history of macaque monkeys. Evolution, 57, 1419–1435.PubMedGoogle Scholar
  34. Young, C. C. (1934). On the Insectivora, Chiroptera, Rodentia and Primates other than Sinanthropus from locality 1 of Choukoutien. Palaeontologia Sinica. Series C, 8, 122–128.Google Scholar

Copyright information

© Springer Science+Business Media, LLC 2009

Authors and Affiliations

  • Tsuyoshi Ito
    • 1
  • Takeshi D. Nishimura
    • 1
  • Brigitte Senut
    • 2
  • Thomas Koppe
    • 3
  • Jacque Treil
    • 4
  • Masanaru Takai
    • 1
  1. 1.Primate Research InstituteKyoto UniversityInuyamaJapan
  2. 2.Département Histoire de la TerreMuséum National d’Histoire Naturelle, USM 203-UMR 5143 CNRSParis Cedex 05France
  3. 3.Department of Anatomy and Cell BiologyErnst-Moritz-Arndt University GreifswaldGreifswaldGermany
  4. 4.UMR 8555 CNRS et Service de Radiologie, Clinique PasteurToulouseFrance

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