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

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Abstract

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.

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Acknowledgments

We wish to sincerely thank Kazumichi Katayama, Masato Nakatsukasa, Toshisada Nishida, and Daisuke Shimizu for their continuous guidance and support throughout the course of this study. We are also grateful to Toshisada Nishida, Editor-in-Chief, and two reviewers for their helpful and constructive comments on this paper. This study was supported by Japan Society for the Promotion of Science (JSPS) Grant-in-Aid for Scientific Research (B) 19370101 to N.O. and in part by the Global Center of Excellence Program A06 “Formation of a Strategic Base for Biodiversity and Evolutionary Research: from Genome to Ecosystem” of the Ministry of Education, Culture, Sports and Technology (MEXT), Japan.

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Author notes

  1. Naomichi Ogihara

    Present address: Department of Mechanical Engineering, Faculty of Science and Technology, Keio University, Yokohama, 223-8522, Japan

Authors and Affiliations

  1. Laboratory of Physical Anthropology, Department of Zoology, Graduate School of Science, Kyoto University, Kitashirakawa-oiwakecho, Sakyo-ku, Kyoto, 606-8502, Japan

    Wataru Yano & Naomichi Ogihara

  2. Primate Research Institute, Kyoto University, 41 Kanrin, Inuyama, 484-8506, Japan

    Naoko Egi

  3. Japan Monkey Centre, 26 Kanrin, Inuyama, 484-0081, Japan

    Tomo Takano

Authors
  1. Wataru Yano
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  2. Naoko Egi
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  3. Tomo Takano
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  4. Naomichi Ogihara
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Corresponding author

Correspondence to Wataru Yano.

Appendix I Specimens used in the present study

Appendix I Specimens used in the present study

ID

Sex

Standardized BPD

Macaca fuscata fucata

 JMC3482

m

0.469

 JMC3484

f

0.554

 JMC1790

m

0.574

 JMC3776

m

0.698

 JMC3195

m

0.671

 JMC1971

f

0.713

 JMC5294

m

0.714

 JMC4562

m

0.718

 JMC3192

f

0.758

 JMC3886

m

0.784

 JMC1401

m

0.759

 JMC3775

m

0.794

 JMC2903

f

0.769

 JMC3783

m

0.830

 JMC3788

f

0.801

 JMC1821

m

0.801

 JMC2361

m

0.860

 JMC3177

m

0.887

Macaca fuscata yakui

 JMC1386

f

0.593

 JMC1574

m

0.684

 JMC2531

f

0.699

 JMC1814

m

0.736

 JMC1500

m

0.731

 JMC4321

m

0.745

 JMC1842

m

0.766

 JMC1535

m

0.828

 JMC1810

m

0.761

 JMC1396

m

0.807

 JMC1791

m

0.807

 JMC3417

m

0.795

 JMC1440

m

0.836

 JMC4415

f

0.946

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Yano, W., Egi, N., Takano, T. et al. Prenatal ontogeny of subspecific variation in the craniofacial morphology of the Japanese macaque (Macaca fuscata). Primates 51, 263–271 (2010). https://doi.org/10.1007/s10329-010-0197-3

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  • DOI: https://doi.org/10.1007/s10329-010-0197-3

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