Table of Contents
Anatomy Research International
Volume 2011, Article ID 484607, 16 pages
http://dx.doi.org/10.1155/2011/484607
Research Article

Making Space for Permanent Molars in Growing Baboon (Papio anubis) and Great Ape (Pan paniscus and P. troglodytes) Mandibles: Possible Ontogenetic Strategies and Solutions

Department of Anatomy and Cell Biology, University of Saskatchewan, Health Sciences Building B328, 107 Wiggins Road, Saskatoon, SK, Canada S7K 5E5

Received 15 December 2010; Accepted 2 March 2011

Academic Editor: Anne M. Burrows

Copyright © 2011 Julia C. Boughner. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. S. W. Oka and B. S. Kraus, “The circumnatal status of molar crown maturation among the hominoidea,” Archives of Oral Biology, vol. 14, no. 6, pp. 639–659, 1969. View at Google Scholar · View at Scopus
  2. A. D. Beynon, M. C. Dean, and D. J. Reid, “Histological study on the chronology of the developing dentition in gorilla and orangutan,” American Journal of Physical Anthropology, vol. 86, no. 2, pp. 189–203, 1991. View at Google Scholar · View at Scopus
  3. L. A. Winkler, J. H. Schwartz, and D. R. Swindler, “Aspects of dental development in the orangutan prior to eruption of the permanent dentition,” American Journal of Physical Anthropology, vol. 86, no. 2, pp. 255–271, 1991. View at Google Scholar · View at Scopus
  4. R. L. Anemone, E. S. Watts, and D. R. Swindler, “Dental development of known-age chimpanzees, Pan troglodytes (primates, pongidae),” American Journal of Physical Anthropology, vol. 86, no. 2, pp. 229–241, 1991. View at Google Scholar · View at Scopus
  5. L. A. Winkler, J. H. Schwartz, and D. R. Swindler, “Development of the orangutan permanent dentition: assessing patterns and variation in tooth development,” American Journal of Physical Anthropology, vol. 99, no. 1, pp. 205–220, 1996. View at Google Scholar · View at Scopus
  6. L. A. Winkler, “A comparison of radiographic and anatomical evidence of tooth development in infant apes,” Folia Primatologica, vol. 65, no. 1, pp. 1–13, 1995. View at Google Scholar · View at Scopus
  7. D. R. Swindler and A. D. Beynon, “The development and microstructure of the dentition of Theropithecus,” in Theropithecus: The Rise and Fall of a Primate Genus, N. G. Jablonski, Ed., pp. 351–381, Cambridge University Press, Cambridge, UK, 1993. View at Google Scholar
  8. W. Dirks, “Histological reconstruction of dental development and age at death in a juvenile gibbon (Hylobates lar),” Journal of Human Evolution, vol. 35, no. 4-5, pp. 411–425, 1998. View at Publisher · View at Google Scholar · View at Scopus
  9. J. C. Boughner and M. C. Dean, “Does space in the jaw influence the timing of molar crown initiation? A model using baboons (Papio anubis) and great apes (Pan troglodytes, Pan paniscus),” Journal of Human Evolution, vol. 46, no. 3, pp. 255–277, 2004. View at Google Scholar · View at Scopus
  10. M. M. Smith and M. I. Coates, “Evolutionary origins of the vertebrate dentition: phylogenetic patterns and developmental evolution,” European Journal of Oral Sciences, vol. 106, no. 1, pp. 482–500, 1998. View at Google Scholar · View at Scopus
  11. G. J. Fraser, C. D. Hulsey, R. F. Bloomquist, K. Uyesugi, N. R. Manley, and J. T. Streelman, “An ancient gene network is co-opted for teeth on old and new jaws,” PLoS Biology, vol. 7, no. 2, Article ID e1000031, 2009. View at Publisher · View at Google Scholar · View at Scopus
  12. A. Huysseune, J.-Y. Sire, and P. E. Witten, “Evolutionary and developmental origins of the vertebrate dentition,” Journal of Anatomy, vol. 214, no. 4, pp. 465–476, 2009. View at Publisher · View at Google Scholar · View at Scopus
  13. M. M. Smith and M. I. Coates, “Evolutionary origins of teeth and jaws: developmental models and phylogenetic patterns,” in Development, Function and Evolution of Teeth, M. F. Teaford, M. M. Smith, and M. W. J. Ferguson, Eds., pp. 133–151, Cambridge University Press, Cambridge, UK, 2000. View at Google Scholar
  14. Y. Shigetani, F. Sugahara, Y. Kawakami, Y. Murakami, S. Hirano, and S. Kuratani, “Heterotopic shift of epithelial-mesenchymal interactions in vertebrate jaw evolution,” Science, vol. 296, no. 5571, pp. 1316–1319, 2002. View at Publisher · View at Google Scholar · View at Scopus
  15. L. Humphrey, “Relative mandibular growth in humans, gorillas and chimpanzees,” in Human Growth in the Past: Studies from Bones and Teeth, R. D. Hoppa and C. M. FitzGerald, Eds., pp. 65–87, Cambridge University Press, Cambridge, UK, 1999. View at Google Scholar
  16. C. T. James, A. Ohazama, A. S. Tucker, and P. T. Sharpe, “Tooth development is independent of a Hox patterning programme,” Developmental Dynamics, vol. 225, no. 3, pp. 332–335, 2002. View at Publisher · View at Google Scholar · View at Scopus
  17. M. McCollum and P. T. Sharpe, “Evolution and development of teeth,” Journal of Anatomy, vol. 199, no. 1-2, pp. 153–159, 2001. View at Publisher · View at Google Scholar · View at Scopus
  18. M. A. McCollum, “The robust australopithecine face: a morphogenetic perspective,” Science, vol. 284, no. 5412, pp. 301–305, 1999. View at Google Scholar · View at Scopus
  19. M. A. McCollum and P. T. Sharpe, “Developmental genetics and early hominid craniodental evolution,” BioEssays, vol. 23, no. 6, pp. 481–493, 2001. View at Publisher · View at Google Scholar · View at Scopus
  20. D. J. Daegling, “Growth in the mandibles of African apes,” Journal of Human Evolution, vol. 30, no. 4, pp. 315–341, 1996. View at Publisher · View at Google Scholar · View at Scopus
  21. A. B. Taylor and C. P. Groves, “Patterns of mandibular variation in Pan and Gorilla and implications for African ape taxonomy,” Journal of Human Evolution, vol. 44, no. 5, pp. 529–561, 2003. View at Publisher · View at Google Scholar · View at Scopus
  22. M. L. Moss, “Functional cranial analysis of mammalian mandibular ramal morphology,” Acta Anatomica, vol. 71, no. 3, pp. 423–447, 1968. View at Google Scholar
  23. M. L. Moss, “A functional analysis of human mandibular growth,” The Journal of Prosthetic Dentistry, vol. 10, no. 6, pp. 1149–1159, 1960. View at Google Scholar · View at Scopus
  24. H. Fukase and G. Suwa, “Influence of size and placement of developing teeth in determining anterior corpus height in prehistoric Jomon and modern Japanese mandibles,” Anthropological Science, vol. 118, no. 2, pp. 75–86, 2010. View at Publisher · View at Google Scholar
  25. W. Dirks, D. J. Reid, C. J. Jolly, J. E. Phillips-Conroy, and F. L. Brett, “Out of the mouths of baboons: stress, life history, and dental development in the Awash National Park hybrid zone, Ethiopia,” American Journal of Physical Anthropology, vol. 118, no. 3, pp. 239–252, 2002. View at Publisher · View at Google Scholar · View at Scopus
  26. D. J. Reid, G. T. Schwartz, C. Dean, and M. S. Chandrasekera, “A histological reconstruction of dental development in the common chimpanzee, Pan troglodytes,” Journal of Human Evolution, vol. 35, no. 4-5, pp. 427–448, 1998. View at Publisher · View at Google Scholar · View at Scopus
  27. P. D Jenkins, Catalogue of Primates in the British Museum (Natural History) Part V: The Apes, Superfamily Hominoidea, Natural History Museum, London, UK, 1990.
  28. P. H. Napier, Catalogue of Primates in the British Museum (Natural History) Part II: Family Cercopithecoidea, Subfamily Cercopithecinae, Natural History Museum, London, UK, 1981.
  29. J. C. Boughner, Dental and Mandibular Growth in Papio and Pan, Ph.D. thesis, University College London (University of London), London, UK, 2002.
  30. F. L. Bookstein, Morphometric Tools for Landmark Data: Geometry and Biology, Cambridge University Press, Cambridge, UK, 1991.
  31. I. L. Dryden and K. V. Mardia, Statistical Shape Analysis, John Wiley & Sons, London, UK, 1st edition, 1998.
  32. L. F. Marcus, M. Corti, A. Loy, G. J. P. Naylor, and D. E. Slice, Advances in Morphometrics, Plenum Press, New York, NY, USA, 1996.
  33. P. O'Higgins and N. Jones, “Facial growth in Cercocebus torquatus: an application of three-dimensional geometric morphometric techniques to the study of morphological variation,” Journal of Anatomy, vol. 193, part 2, pp. 251–272, 1998. View at Publisher · View at Google Scholar · View at Scopus
  34. D. Slice, GRF-ND Generalized Rotational Fitting of N-Dimensional Landmark Data, Department of Ecology and Evolution, State University of New York, Stony Brook, NY, USA, 1993.
  35. F. J. Rohlf and D. Slice, “Extensions of the Procrustes method for the optimal superimposition of landmarks,” Systematic Zoology, vol. 39, no. 1, pp. 40–59, 1990. View at Google Scholar
  36. C. R. Goodall, “Procrustes methods in the statistical analysis of shape,” Journal of the Royal Statistical Society, vol. 53, no. 2, pp. 285–339, 1991. View at Google Scholar
  37. M. Collard and P. O'Higgins, “Ontogeny and homoplasy in the papionin monkey face,” Evolution and Development, vol. 3, no. 5, pp. 322–331, 2001. View at Publisher · View at Google Scholar · View at Scopus
  38. S. K. Lee, Y. S. Kim, H. S. Oh, K. H. Yang, E. C. Kim, and J. G. Chi, “Prenatal development of the human mandible,” Anatomical Record, vol. 263, no. 3, pp. 314–325, 2001. View at Google Scholar · View at Scopus
  39. Y. P. Liu, R. G. Behrents, and P. H. Buschang, “Mandibular growth, remodeling, and maturation during infancy and early childhood,” Angle Orthodontist, vol. 80, no. 1, pp. 97–105, 2010. View at Publisher · View at Google Scholar · View at Scopus
  40. R. J. Radlanski, H. Renz, and M. C. Klarkowski, “Prenatal development of the human mandible. 3D reconstructions, morphometry and bone remodelling pattern, sizes 12–117 mm CRL,” Anatomy and Embryology, vol. 207, no. 3, pp. 221–232, 2003. View at Publisher · View at Google Scholar · View at Scopus
  41. G. E. Wise and G. J. King, “Mechanisms of tooth eruption and orthodontic tooth movement,” Journal of Dental Research, vol. 87, no. 5, pp. 414–434, 2008. View at Publisher · View at Google Scholar · View at Scopus
  42. S. Hartwig-Scherer and R. D. Martin, “Allometry and prediction in hominoids: a solution to the problem of intervening variables,” American Journal of Physical Anthropology, vol. 88, no. 1, pp. 37–57, 1992. View at Publisher · View at Google Scholar · View at Scopus
  43. J. C. Boughner and M. C. Dean, “Mandibular shape, ontogeny and dental development in bonobos (Pan paniscus) and Chimpanzees (Pan troglodytes),” Evolutionary Biology, vol. 35, no. 4, pp. 296–308, 2008. View at Publisher · View at Google Scholar · View at Scopus
  44. B. H. Smith, T. L. Crummett, and K. L. Brandt, “Ages of eruption of primate teeth: a compendium for aging individuals and comparing life histories,” American Journal of Physical Anthropology, vol. 37, supplement 19, pp. 177–231, 1994. View at Google Scholar · View at Scopus
  45. D. R. Swindler and D. Meekins, “Dental development of the permanent mandibular teeth in the baboon, Papio cynocephalus,” American Journal of Human Biology, vol. 3, no. 6, pp. 571–580, 1991. View at Google Scholar
  46. V. S. Aggarwal, C. Carpenter, L. Freyer, J. Liao, M. Petti, and B. E. Morrow, “Mesodermal Tbx1 is required for patterning the proximal mandible in mice,” Developmental Biology, vol. 344, no. 2, pp. 669–681, 2010. View at Publisher · View at Google Scholar · View at Scopus
  47. M. Mina, Y. H. Wang, A. M. Ivanisevic, W. B. Upholt, and B. Rodgers, “Region- and stage-specific effects of FGFs and BMPs in chick mandibular morphogenesis,” Developmental Dynamics, vol. 223, no. 3, pp. 333–352, 2002. View at Publisher · View at Google Scholar · View at Scopus
  48. S. Creuzet, G. Couly, C. Vincent, and N. M. Le Douarin, “Negative effect of Hox gene expression on the development of the neural crest-derived facial skeleton,” Development, vol. 129, no. 18, pp. 4301–4313, 2002. View at Google Scholar · View at Scopus
  49. A. Trumpp, M. J. Depew, J. L. R. Rubenstein, J. M. Bishop, and G. R. Martin, “Cre-mediated gene inactivation demonstrates that FGF8 is required for cell survival and patterning of the first branchial arch,” Genes and Development, vol. 13, no. 23, pp. 3136–3148, 1999. View at Publisher · View at Google Scholar · View at Scopus
  50. A. S. Tucker, G. Yamada, M. Grigoriou, V. Pachnis, and P. T. Sharpe, “Fgf-8 determines rostral-caudal polarity in the first branchial arch,” Development, vol. 126, no. 1, pp. 51–61, 1999. View at Google Scholar · View at Scopus
  51. W. R. Atchley and B. K. Hall, “A model for development and evolution of complex morphological structures,” Biological Reviews of the Cambridge Philosophical Society, vol. 66, no. 2, pp. 101–157, 1991. View at Google Scholar · View at Scopus
  52. J. Kieser, “Biomechanics of masticatory force production,” Journal of Human Evolution, vol. 36, no. 5, pp. 575–579, 1999. View at Google Scholar · View at Scopus
  53. W. L. Hylander, “Mandibular function and biomechanical stress and scaling,” American Zoologist, vol. 25, no. 2, pp. 315–330, 1985. View at Publisher · View at Google Scholar
  54. M. A. Spencer and B. Demes, “Biomechanical analysis of masticatory system configuration in neandertals and inuits,” American Journal of Physical Anthropology, vol. 91, no. 1, pp. 1–20, 1993. View at Google Scholar · View at Scopus
  55. T. G. Boyd, W. A. Castelli, and D. F. Huelke, “Removal of the temporalis muscle from its origin: effects on the size and shape of the coronoid process,” Journal of Dental Research, vol. 46, no. 5, pp. 997–1001, 1967. View at Google Scholar · View at Scopus
  56. S. L. Horowitz and H. H. Shapiro, “Modification of skull and jaw architecture following removal of the masseter muscle in the rat,” American Journal of Physical Anthropology, vol. 13, no. 2, pp. 301–308, 1955. View at Google Scholar · View at Scopus
  57. N. Hunt, “Muscle function and the control of facial form,” in Clinical Oral Science, M. Harris, M. Edgar, and S Meghji, Eds., pp. 120–133, Wright, Oxford, UK, 1998. View at Google Scholar
  58. S. Kiliaridis, C. Mejersjö, and B. Thilander, “Muscle function and craniofacial morphology: a clinical study in patients with myotonic dystrophy,” European Journal of Orthodontics, vol. 11, no. 2, pp. 131–138, 1989. View at Google Scholar · View at Scopus
  59. S. K. Nanda, W. W. Merow, and V. Sassouni, “Repositioning of the masseter muscle and its effect on skeletal form and structure,” Angle Orthodontist, vol. 37, no. 4, pp. 304–308, 1967. View at Google Scholar · View at Scopus
  60. A. B. Taylor, “Masticatory form and function in the African apes,” American Journal of Physical Anthropology, vol. 117, no. 2, pp. 133–156, 2002. View at Publisher · View at Google Scholar · View at Scopus
  61. S. C. Antón, “Cranial adaptation to a high attrition diet in Japanese macaques,” International Journal of Primatology, vol. 17, no. 3, pp. 401–427, 1996. View at Google Scholar · View at Scopus
  62. E. L. du Brul, “Early hominid feeding mechanisms,” American Journal of Physical Anthropology, vol. 47, no. 2, pp. 305–320, 1977. View at Google Scholar · View at Scopus
  63. J. W. Osborn, “Relationship between the mandibular condyle and the occlusal plane during hominid evolution: some of its effects on jaw mechanics,” American Journal of Physical Anthropology, vol. 73, no. 2, pp. 193–207, 1987. View at Google Scholar · View at Scopus
  64. G. S. Throckmorton, R. A. Finn, and W. H. Bell, “Biomechanics of differences in lower facial height,” American Journal of Orthodontics, vol. 77, no. 4, pp. 410–420, 1980. View at Google Scholar · View at Scopus
  65. S. C. Antón, “Macaque masseter muscle: internal architecture, fiber length and cross-sectional area,” International Journal of Primatology, vol. 20, no. 3, pp. 441–462, 1999. View at Google Scholar · View at Scopus
  66. R. K. Malenky and R. W. Wrangham, “A quantitative comparison of terrestrial herbaceous food consumption by Pan paniscus in the Lomako Forest, Zaire, and Pan troglodytes in the Kibale Forest, Uganda,” American Journal of Primatology, vol. 32, no. 1, pp. 1–12, 1994. View at Google Scholar · View at Scopus
  67. R. K. Malenky, S. Kuroda, E. O. Vineberg, and R. W. Wrangham, “The significance of terrestrial herbaceous foods for bonobos, chimpanzees and gorillas,” in Chimpanzee Cultures, R. W. Wrangham, W. C. McGrew, F. B. M deWaal, and P. G. Heltne, Eds., pp. 59–75, Chicago Academy of Sciences, Chicago, Ill, USA, 1994. View at Google Scholar
  68. R. W. Wrangham, C. A. Chapman, and L. J. Chapman, “Seed dispersal by forest chimpanzees in Uganda,” Journal of Tropical Ecology, vol. 10, no. 3, pp. 355–368, 1994. View at Google Scholar · View at Scopus
  69. M. A. McCollum, “Rethinking incisor size and diet in anthropoids: diet, incisor wear and incisor breadth in the African apes,” American Journal of Physical Anthropology, vol. 133, no. 3, pp. 986–993, 2007. View at Publisher · View at Google Scholar · View at Scopus
  70. M. A. McCollum and W. C McGrew, “Dental evolution in the genus Pan,” American Journal of Physical Anthropology, vol. 114, p. 105, 2001. View at Google Scholar
  71. I. DeVore and S. L. Washburn, “Baboon ecology and human evolution,” in African Ecology and Human Evolution, F. Clark Howell and F. Bourliere, Eds., Viking Fund Publications in Anthropology no. 36, pp. 335–367, Wenner-Gren Foundation for Anthropological Research, London, UK, 1963. View at Google Scholar
  72. S. L. Washburn and I. DeVore, “Social behavior of baboons and early man,” in Social Life of Early Man, S. L. Washburn, Ed., Viking Fund Publications in Anthropology no. 31, pp. 91–105, Aldine Publishing Company, Chicago, Ill, USA, 1961. View at Google Scholar
  73. T. E. Rowell, “Forest living baboons in Uganda,” Journal of Zoology, vol. 149, no. 3, pp. 344–364, 1966. View at Google Scholar
  74. T. Orliaguet, P. Dechelotte, T. Scheye, and G. Vanneuville, “Relations between Meckel's cartilage and the morphogenesis of the mandible in the human embryo,” Surgical and Radiologic Anatomy, vol. 15, no. 1, pp. 41–46, 1993. View at Google Scholar · View at Scopus
  75. J. M. Smartt Jr., D. W. Low, and S. P. Bartlett, “The pediatric mandible: I. A primer on growth and development,” Plastic and Reconstructive Surgery, vol. 116, no. 1, pp. 14e–23e, 2005. View at Publisher · View at Google Scholar · View at Scopus
  76. Y. Kitahara, N. Suda, T. Kuroda, F. Beck, V. E. Hammond, and Y. Takano, “Disturbed tooth development in parathyroid hormone-related protein (PTHrP)-gene knockout mice,” Bone, vol. 30, no. 1, pp. 48–56, 2002. View at Publisher · View at Google Scholar · View at Scopus
  77. Y. Kitahara, N. Suda, T. Terashima et al., “Accelerated bone formation and increased osteoblast number contribute to the abnormal tooth germ development in parathyroid hormone-related protein knockout mice,” Bone, vol. 35, no. 5, pp. 1100–1106, 2004. View at Publisher · View at Google Scholar · View at Scopus
  78. K. Mekaapiruk, N. Suda, V. E. Hammond et al., “The influence of parathyroid hormone-related protein (PTHrP) on tooth-germ development and osteoclastogenesis in alveolar bone of PTHrP-knock out and wild-type mice in vitro,” Archives of Oral Biology, vol. 47, no. 9, pp. 665–672, 2002. View at Publisher · View at Google Scholar · View at Scopus
  79. Z. Sun and B. C. Tee, “Molecular variations related to the regional differences in periosteal growth at the mandibular ramus,” Anatomical Record, vol. 294, no. 1, pp. 79–87, 2011. View at Publisher · View at Google Scholar
  80. A. L. Lerner and J. L. Kuhn, “Characterization of regional and age-related variations in the growth of the rabbit distal femur,” Journal of Orthopaedic Research, vol. 15, no. 3, pp. 353–361, 1997. View at Publisher · View at Google Scholar · View at Scopus
  81. M. A. Serrat, C. O. Lovejoy, and D. King, “Age- and site-specific decline in insulin-like growth factor-I receptor expression is correlated with differential growth plate activity in the mouse hindlimb,” Anatomical Record, vol. 290, no. 4, pp. 375–381, 2007. View at Publisher · View at Google Scholar
  82. A. L. Lerner, J. L. Kuhn, and S. J. Hollister, “Are regional variations in bone growth related to mechanical stress and strain parameters?” Journal of Biomechanics, vol. 31, no. 4, pp. 327–335, 1998. View at Publisher · View at Google Scholar · View at Scopus
  83. Q. Wang, D. W. Ashley, and P. C. Dechow, “Regional, ontogenetic, and sex-related variations in elastic properties of cortical bone in baboon mandibles,” American Journal of Physical Anthropology, vol. 141, no. 4, pp. 526–549, 2010. View at Publisher · View at Google Scholar · View at Scopus