Phenotypic plasticity in the mandibular morphology of Japanese macaques: captive–wild comparison

Abstract

Despite the accumulating evidence suggesting the importance of phenotypic plasticity in diversification and adaptation, little is known about plastic variation in primate skulls. The present study evaluated the plastic variation of the mandible in Japanese macaques by comparing wild and captive specimens. The results showed that captive individuals are square-jawed with relatively longer tooth rows than wild individuals. We also found that this shape change resembles the sexual dimorphism, indicating that the mandibles of captive individuals are to some extent masculinized. By contrast, the mandible morphology was not clearly explained by ecogeographical factors. These findings suggest the possibility that perturbations in the social environment in captivity and resulting changes of androgenic hormones may have influenced the development of mandible shape. As the high plasticity of social properties is well known in wild primates, social environment may cause the inter- and intra-population diversity of skull morphology, even in the wild. The captive–wild morphological difference detected in this study, however, can also be possibly formed by other untested sources of variation (e.g. inter-population genetic variation), and therefore this hypothesis should be validated further.

Cranial morphology of captive mammals: a meta-analysis

“…The skulls of captive mammals may differ from wild populations in both size and shape (e.g., [ 46 , 88 , 110 , 120 ]). Documented differences include changes in the cranial length and width of African lions ( Panthera leo [ 43 , 46 ];), sagittal crest height of Amur tigers ( P. tigris [ 28 ];), and mandibular morphology of Japanese macaques ( Macaca fuscata [ 50 ];), traits which are integral for feeding and influence bite force and dietary niche [ 77 , 79 , 108 , 122 ]. The relative spread of the zygomatic arch is highly indicative of cranial musculature and functionality, where a wider zygomatic arch implies the presence of enhanced musculature and a stronger bite force often associated with carnivores (e.g., [ 24 , 43 ]) and gnawing rodents (e.g., [ 30 ]).…”

“…Lynch & Hayden [ 63 ] suggested the cranial changes they observed among farmed American mink ( Mustela vison ) were largely the result of differing selection pressures. Abnormal skull morphology of several captive mammals, including coyotes ( Canis latrans [ 24 ];), African lions ( Panthera leo [ 43 ];), and Japanese macaques ( Macaca fuscata [ 50 ];) have all largely been attributed to phenotypic plasticity.…”

“…For example, while African lions tend to show rather drastic, consistent morphological changes associated with an increase in zygomatic breadth [ 43 , 46 , 125 ], house mice ( Mus musculus ) show little morphological change in captivity [ 23 ]. Even closely related taxa may differ in the degree of change that they exhibit once in captivity [ 38 , 50 , 97 ], possibly due to species ecology where certain traits may predispose a particular species to a specific captive response. The likelihood of morphological changes occurring in captivity may increase when an animal’s habitat is difficult to replicate (leading to heightened stress behaviors) or when diets are difficult to accommodate [ 18 , 24 , 56 ].…”

Tooth chipping prevalence and patterns in extant primates

“…), Raffles' banded langurs ( Presbytis femoralis ), Mentawai langurs ( P. potenziani ), brown woolly monkeys ( Lagothrix lagothricha ) and sakis ( Pithecia sp. ), curated at the Primate Research Institute, Kyoto University (Buck et al, 2018; Kamaluddin et al, 2019). Chimpanzees ( Pan troglodytes ) and Western lowland gorillas ( Gorilla gorilla gorilla ), curated at the Powell‐Cotton Museum, UK, were also included (Towle et al, 2017).…”

Subspecies and sexual craniofacial size and shape variations in Japanese macaques (<i>Macaca fuscata</i>)

“…We carefully inspected cranial specimens to exclude broken and/or pathological samples, and a total of 55 adult dried crania of Japanese macaque (14 male MFFs, 13 female MFFs, 14 male MFYs, and 14 female MFYs) were obtained from the Laboratory of Physical Anthropology, Kyoto University (LPA; Kyoto, Japan), the Primate Research Institute, Kyoto University (PRI; Inuyama, Japan), and the Japan Monkey Centre (JMC; Inuyama, Japan). Since wild and captive Japanese macaques do not differ significantly (Kamaluddin et al, 2019), we employed mixed samples of wild and captive origin as well as a few samples of unknown origin from animal traders. We carefully used unbiased numbers for the different groups (Table 1).…”