, Volume 51, Issue 3, pp 263–271 | Cite as

Prenatal ontogeny of subspecific variation in the craniofacial morphology of the Japanese macaque (Macaca fuscata)

  • Wataru Yano
  • Naoko Egi
  • Tomo Takano
  • Naomichi Ogihara
Original Article


We cross-sectionally investigated prenatal ontogeny of craniofacial shape in the two subspecies of the Japanese macaque (Macaca fuscata fuscata and Macaca fuscata yakui) using a geometric morphometric technique to explore the process of morphogenetic divergence leading to the adult morphological difference between the subspecies. The sample comprised a total of 32 formalin-fixed fetal specimens of the two subspecies, in approximately the second and third trimesters. Each fetal cranium was scanned using computed tomography to generate a three-dimensional surface model, and 68 landmarks were digitized on the external and internal surface of each cranium to trace the growth-related changes in craniofacial shape of the two subspecies. The results of our study demonstrated that the two subspecies generally shared the same craniofacial growth pattern. Both crania tend to exhibit relative contraction of the neurocranium in the mediolateral and superoinferior directions, a more superiorly positioned cranial base, a more vertically oriented occipital squama, and a more anteriorly positioned viscerocranium as the cranial size increased. However, distinctive subspecific differences, for example relatively narrower orbital breadth, higher orbit, higher position of the nuchal crest, and more protrudent snout found in Macaca fuscata yakui were already present during the prenatal period. This study demonstrated that morphological differentiation in the craniofacial shape may occur at a very early stage of the fetal period even between closely related subspecies of the Japanese macaque.


Three-dimensional morphometrics Skull Development Fetus Ontogenetic trajectory 


  1. Ackermann RR, Krovitz GE (2002) Common patterns of facial ontogeny in the hominid lineage. Anat Rec 269:142–147CrossRefPubMedGoogle Scholar
  2. Antón SC (1996) Cranial adaptation to a high attrition diet in Japanese macaques. Int J Primatol 17:401–427CrossRefGoogle Scholar
  3. Bastir M, Rosas A (2009) Mosaic evolution of the basicranium in Homo and its relation to modular development. Evol Biol 36:57–70CrossRefGoogle Scholar
  4. Bastir M, O’Higgins P, Rosas A (2007) Facial ontogeny in Neanderthals and modern humans. Proc R Soc Lond B 274:1125–1132CrossRefGoogle Scholar
  5. Berge C, Penin X (2004) Ontogenetic allometry, heterochrony, and interspecific differences in the skull of African apes, using tridimensional Procrustes analysis. Am J Phys Anthropol 124:124–138CrossRefPubMedGoogle Scholar
  6. Bulygina E, Mitteroecker P, Aiello L (2006) Ontogeny of facial dimorphism and patterns of individual development within one human population. Am J Phys Anthropol 131:432–443CrossRefPubMedGoogle Scholar
  7. Cobb SN, O’Higgins P (2004) Hominins do not share a common postnatal facial ontogenetic shape trajectory. J Exp Zool B Mol Dev Evol 302B:302–321CrossRefGoogle Scholar
  8. Cobb SN, O’Higgins P (2007) The ontogeny of sexual dimorphism in the facial skeleton of the African apes. J Hum Evol 53:176–190CrossRefPubMedGoogle Scholar
  9. Grafen A, Hails R (2002) Modern statistics for the life sciences. Oxford University Press, OxfordGoogle Scholar
  10. Hamada Y, Watanabe T, Iwamoto M (1996) Morphological variations among local populations of Japanese macaque (Macaca fuscata). In: Shotake T, Wada K (eds) Variations in the Asian Macaques. Tokai University Press, Tokyo, pp 97–115Google Scholar
  11. Hayasaka K, Kawamoto Y, Shotake T, Nozawa K (1987) Population genetical study of Japanese macaques, Macaca fuscata, I the Shimokita A1 troop, with relationships to Japanese macaques in other troops. Primates 28:507–516CrossRefGoogle Scholar
  12. Ikeda J, Watanabe T (1966) Morphological studies of Macaca fuscata: III. Craniometry. Primates 7:271–288CrossRefGoogle Scholar
  13. Iwamoto M (1971) Morphological studies of Macaca fuscata: IV Somatometry. Primates 12:151–174CrossRefGoogle Scholar
  14. Jeffery N (2003) Brain expansion and comparative prenatal ontogeny of the non-hominoid primate cranial base. J Hum Evol 45:263–284CrossRefPubMedGoogle Scholar
  15. Jeffery N, Spoor C (2002) Brain size and the human cranial base: a prenatal perspective. Am J Phys Anthropol 118:324–340CrossRefPubMedGoogle Scholar
  16. Jeffery N, Spoor C (2004) Ossification and midline shape changes of the human fetal cranial base. Am J Phys Anthropol 123:78–90CrossRefPubMedGoogle Scholar
  17. Jeffery N, Davies K, Kockenberger W, Williams S (2007) Craniofacial growth in fetal Tarsius bancanus: brains, eyes and nasal septa. J Anat 210:703–722CrossRefPubMedGoogle Scholar
  18. Joffe TH, Tarantal AF, Rice K, Leland M, Oerke AK, Rodeck C, Geary M, Hindmarsh P, Wells JCK, Aiello LC (2004) Fetal and infant head circumference sexual dimorphism in primates. Am J Phys Anthropol 126:97–110CrossRefGoogle Scholar
  19. Klingenberg CP, Mebus K, Auffray JC (2003) Developmental integration in a complex morphological structure: how distinct are the modules in the mouse mandible? Evol Dev 5:522–531CrossRefPubMedGoogle Scholar
  20. Kvinnsland S (1971) The sagittal growth of the foetal cranial base. Acta Odontol Scand 29:699–715CrossRefPubMedGoogle Scholar
  21. Leigh SR (2006) Cranial ontogeny of Papio Baboons (Papio hamadryas). Am J Phys Anthropol 130:71–84CrossRefPubMedGoogle Scholar
  22. Marmi J, Bertranpetit J, Terradas J, Takenaka O, Domingo-Roura X (2004) Radiation and phylogeny in the Japanese macaque, Macaca fuscata. Mol Phylogenet Evol 30:676–685CrossRefPubMedGoogle Scholar
  23. Mitteroecker P, Gunz P, Bernard M, Schaefer K, Bookstein FL (2004) Comparison of cranial ontogenetic trajectories among great apes and humans. J Hum Evol 46:679–697CrossRefPubMedGoogle Scholar
  24. Morimoto N, Ogihara N, Katayama K, Shiota K (2008) Three-dimensional ontogenetic shape changes in the human cranium during the fetal period. J Anat 212:627–635CrossRefPubMedGoogle Scholar
  25. Nozawa K, Shotake T, Minezawa M, Kawamoto Y, Hayasaka K, Kawamoto S (1991) Population genetics of Japanese monkeys: III Ancestry and differentiation of local populations. Primates 32:411–435CrossRefGoogle Scholar
  26. O’Higgins P, Collard M (2002) Sexual dimorphism and facial growth in the papionin monkeys. J Zool 257:255–272CrossRefGoogle Scholar
  27. O’Higgins P, Jones N (1998) Facial growth in Cercocebus torquatus: an application of three dimensional geometric morphometric techniques to the study of morphological variation. J Anat 193:251–272CrossRefPubMedGoogle Scholar
  28. O’Higgins P, Jones N (2006) Tools for statistical shape analysis. Hull York Medical School available from:
  29. O’Higgins P, Chadfield P, Jones N (2001) Facial growth and the ontogeny of morphological variation within and between Cebus apella and Cercocebus torquatus. J Zool 254:337–357CrossRefGoogle Scholar
  30. Ponce de León MS, Zollikofer CPE (2001) Neanderthal cranial ontogeny and its implications for late hominid diversity. Nature 412:534–538CrossRefPubMedGoogle Scholar
  31. Ravosa MJ (1991) The ontogeny of cranial sexual dimorphism in two Old World monkeys: Macaca fascicularis (Cercopithecine) and Nasalis larvatus (Colobinae). Int J Primatol 12:403–426CrossRefGoogle Scholar
  32. Richtsmeier JT, Corner BD, Grausz HM, Cheverud JM, Danahey SE (1993) The role of postnatal growth pattern in the production of facial morphology. Syst Biol 42:307–330Google Scholar
  33. Sirianni JE, Newell-Morris L (1980) Craniofacial growth of fetal Macaca nemestrina: a cephalometric roentgenographic study. Am J Phys Anthropol 53:407–421CrossRefPubMedGoogle Scholar
  34. Sirianni JE, van Ness AL (1978) Postnatal growth of the cranial base in Macaca nemestrina. Am J Phys Anthropol 49:329–339CrossRefPubMedGoogle Scholar
  35. Sirianni JE, Newell-Morris L, Campbell M (1981) Growth of the fetal pigtailed macaque (Macaca nemestrina) I Cephalofacial dimensions. Folia Primatol 35:65–75CrossRefPubMedGoogle Scholar
  36. Swindler DR, McCoy HA (1964) Calcification of deciduous teeth in rhesus monkeys. Science 144:1243–1244CrossRefPubMedGoogle Scholar
  37. Viðarsdóttir US, O’Higgins P, Stringer C (2002) A geometric morphometric study of regional differences in the ontogeny of the modern human facial skeleton. J Anat 201:211–229CrossRefGoogle Scholar
  38. Zollikofer CPE, Ponce de León MS (2002) Visualizing patterns of craniofacial shape variation in Homo sapiens. Proc R Soc Lond B 269:801–807CrossRefGoogle Scholar
  39. Zumpano MP, Richtsmeier JT (2003) Growth-related shape changes in the fetal craniofacial complex of humans (Homo sapiens) and pigtailed macaques (Macaca nemestrina): a 3D-CT comparative analysis. Am J Phys Anthropol 120:339–351CrossRefPubMedGoogle Scholar

Copyright information

© Japan Monkey Centre and Springer 2010

Authors and Affiliations

  • Wataru Yano
    • 1
  • Naoko Egi
    • 2
  • Tomo Takano
    • 3
  • Naomichi Ogihara
    • 1
    • 4
  1. 1.Laboratory of Physical Anthropology, Department of Zoology, Graduate School of ScienceKyoto UniversityKyotoJapan
  2. 2.Primate Research InstituteKyoto UniversityInuyamaJapan
  3. 3.Japan Monkey CentreInuyamaJapan
  4. 4.Department of Mechanical Engineering, Faculty of Science and TechnologyKeio UniversityYokohamaJapan

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