Macaca Fuscata
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Anthropological Science Vol. 128(2), 71–81, 2020 Subspecies and sexual craniofacial size and shape variations in Japanese macaques (Macaca fuscata) Wataru Yano1*, Naoko Egi2, Tomo Takano3, Naomichi Ogihara4 1Laboratory of Biology, National Defense Medical College, 3-2 Namiki, Tokorozawa, Saitama 359-8513, Japan 2Phylogeny and Systematics section, Primate Research Institute, Kyoto University, Inuyama, Aichi 484-8506, Japan 3Japan Monkey Centre, 26 Kanrin, Inuyama, Aichi 484-0081, Japan 4Laboratory of Human Evolutionary Biomechanics, Department of Biological Sciences, The University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033, Japan Received 16 December 2018; accepted 5 May 2020 Abstract Adaptation to various environments leads to evolutionary change in size and shape in non- human primates. In island environments, larger mammals tend to be smaller compared with the original mainland population. The Japanese macaque (Macaca fuscata) has two subspecies: Macaca fuscata yakui (MFY) on Yakushima Island, and Macaca fuscata fuscata (MFF) on the main Japanese archipelago. Since adult shape differences reflect spatiotemporal developmental pattern differences, it is interesting to examine allometric patterns for groups that show significant size variation. The main purpose of the present study is to quantitatively examine the craniofacial size and three-dimensional sexual and subspecies shape variation, focusing on the effects of size variation on shape variation. Computed to- mography scans of 55 specimens were used to generate a three-dimensional model of each cranium, and 57 landmarks were digitized to quantify the craniofacial shape variation in Japanese macaques. We subsequently employed regression analyses to deduce vectors responsible for allometry, sex, subspecies shape variations, and the influence of size on sexual and subspecies shape variations. The results showed that four intraspecific groups, consisting of two subspecies and the two sexes, significantly differed in both size and shape space. In size, the cranium of MFY was smaller than that of MFF in both sexes, and female crania were smaller than male crania in both subspecies. Allometry as well as sexual dimorphism in shape was related to a relatively broad orbit, smaller neurocranium, enlarged snout, and broader temporal fossa in males. Subspecies shape differences were a relatively narrow and short orbit and sphenoid, smaller neurocranium, and postorbital constriction in MFY. Sexual shape variation was largely associated with size variation. On the other hand, subspecies shape variation was not significantly correlated with size. We discuss these intraspecific cranial size and shape variations and the effect of size on shape variation from evolutional and developmental perspectives. Key words: Macaca fuscata, geometric morphometrics, subspecies, sexual dimorphism, allometry (MFF). Later, molecular phylogenetic analyses demonstrated Introduction that the genetic variation of MFY falls within the range of The Japanese macaque (Macaca fuscata) has the most the MFF population and the subspecific status of MFY has northerly range among extant non-human primates, and is consequently been questioned (blood protein: Nozawa et al., endemic to the Japanese archipelago. Kuroda (1940) first 1991; mtDNA: Marmi et al., 2004; Kawamoto et al., 2007; distinguished a southern population on Yakushima Island Kawamoto, 2010). On the other hand, these molecular (504.9 km2) from other populations based on its reduced analyses revealed the isolation and subsequent unique body size and diagnostic pelage color, and he proposed sub- evolutionary history of MFY. According to Nozawa et al. species recognition of Macaca fuscata yakui (MFY), distinct (1991), MFY and MFF diverged 178 kya ago, and gene flow from their mainland counterpart Macaca fuscata fuscata from the mainland of the Japanese archipelago to Yakushima Island after Marine Isotope Stages (MIS) 6–8 (130–300 kya) is unlikely. Hayaishi and Kawamoto (2006) also showed that * Correspondence to: Wataru Yano, Laboratory of Biology, National Defense Medical College, 3-2 Namiki, Tokorozawa, Saitama 359- there should have been no migration between Yakushima 8513, Japan. and the nearest Kyushu Island of the Japanese mainland. E-mail: [email protected] After divergence, about 7300 years ago the population in Published online 31 July 2020 Yakushima Island suffered from a bottleneck effect due to a in J-STAGE (www.jstage.jst.go.jp) DOI: 10.1537/ase.2005052 massive volcanic explosion 40 km from this island (Hayaishi © 2020 The Anthropological Society of Nippon 71 72 W. YANO ET AL. Anthropological Science and Kawamoto, 2006). of isolated primates in island environments. We discuss the Cranial form differences between MFY and MFF have evolutional and developmental factors responsible for the been diagnosed by using linear distance-based morphometrics variation in cranial size and shape in the Japanese macaque. (craniometry: Ikeda and Watanabe, 1966; Kuroda 1984, 2002; Mouri and Nishimura, 2002; somatometry: Iwamoto, Methods 1971; Hamada et al., 1996). According to these studies on size variation, MFY crania are generally smaller than MFF We carefully inspected cranial specimens to exclude crania. Regarding shape, Ikeda and Watanabe (1966) pointed broken and/or pathological samples, and a total of 55 adult out that MFY has distinct cranial features with expanded dried crania of Japanese macaque (14 male MFFs, 13 female zygoma, postorbital constriction, higher lambda and inion, MFFs, 14 male MFYs, and 14 female MFYs) were obtained narrower orbit, and a protrusive snout. As for sexual shape from the Laboratory of Physical Anthropology, Kyoto Uni- variation, Ikeda and Watanabe (1966) reported that the versity (LPA; Kyoto, Japan), the Primate Research Institute, crania of male Japanese macaques showed a relatively large Kyoto University (PRI; Inuyama, Japan), and the Japan splanchnocranium. However, these studies did not conduct Monkey Centre (JMC; Inuyama, Japan). Since wild and further statistical analysis on the relationship between size captive Japanese macaques do not differ significantly and shape. This is partly due to limitations in conventional (Kamaluddin et al., 2019), we employed mixed samples of morphometrics for quantifying biological form. Linear wild and captive origin as well as a few samples of unknown measurements involve removing any spatial information origin from animal traders. We carefully used unbiased other than the linear distance between two landmarks. Since numbers for the different groups (Table 1). For wild the positional data of each landmark are omitted, the observ- specimens of MFF, we sampled dried crania from a wide er cannot maintain relative spatial relationships (i.e. variety of populations inhabiting the mainland Japanese ar- geometry) between landmarks. For example, even though chipelago. We used only adult specimens who have upper we can detect the increase in cranial length by linear meas- third molars fully erupted. urement, we cannot know if the glabella and/or inion chang- Each specimen was scanned with a computed tomography es their positions. Linear measurement also has limitations (CT) scanner (TSX-002A/4I; Toshiba Medical Systems, in extensive statistical analyses. Once decomposed into a set Tokyo, Japan) in LPA. The tube voltage and current were set of linear dimensions, the integrity of the biological form at 120 kV and 100 mA. Cross-sectional images were recon- decays and subsequent statistical analyses with external structed with a pixel size of 0.20–0.25 mm and a slice inter- variables or visualization of the statistical results can be val of 0.20 mm. The 3D surface of the cranium was then partial and incomplete (Zelditch et al., 2004; Slice, 2005). generated using a triangular mesh model with commercial To rigorously quantify subspecies shape variations, and software (Analyze 6.0; Mayo Clinic, Rochester, MN, USA). the relationship of size and shape variation, we employed We digitized a total of 57 landmarks (Figure 1, Table 2) landmark-based three-dimensional geometric morphomet- on the external and internal surfaces of each cranium using rics (GM). GM enables integrated quantification of biologi- commercial software (Rapidform 2004; INUS Technology, cal form without losing geometric information of landmarks. Seoul, Korea). All the crania were digitized by the same We employed generalized Procrustes analysis (GPA) person (W.Y.). As shape variances due to left–right asymme- (Zelditch et al., 2004; Slice, 2005). In this morphometry, try were not considered here, we symmetrized the positions landmark sets of samples are first normalized, translated to of all landmarks using self-symmetrization (Zollikofer and the same centroid position, scaled into the same centroid Ponce de León, 2002). Specifically, we created the horizon- size, and finally rotated about the centroid using least- tally reflected specimen for each sample and superimposed squares fitting. The coordinate data of landmark sets after them by least-squares superposition to calculate the mean of fitting denotes its intrinsic shape. Since the original centroid each landmark coordinate, yielding the symmetrized speci- position, centroid size, and rotation angle about centroid are men of the original. retrievable, we can use them as external parameters as well. Then we analyzed the variances in the landmark positions Furthermore, since the composition of a set of landmarks is using the geometric morphometric software Morphologika unchanged,