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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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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Keywords

  • Three-dimensional morphometrics
  • Skull
  • Development
  • Fetus
  • Ontogenetic trajectory