skip to main content


Title: Postcranial Skeletal Differences in Free‐Range and Captive‐Born Primates
ABSTRACT

Skeletal morphology is important in evolutionary, genetic, developmental, physiological, and functional studies. Although samples from free‐ranging individuals may be preferable, constraints of sample size, demography, or conservation status may necessitate the inclusion of captive‐born individuals. Captivity may be associated with physical, physiological, or behavioral differences that may affect skeletal form. This study assesses differences in postcranial skeletal form between free‐range and captive‐bornMacaca mulattaandSaguinus oedipus. Samples included free‐rangeM. mulattafrom Cayo Santiago (Caribbean Primate Research Center) and captive‐born macaques from the Wisconsin National Primate Research Center.S. oedipussamples included free‐range born and captive‐born individuals from the Oak Ridge Associated Universities Marmoset Research Center. Twenty‐four dimensions of various bones, including the scapula, upper limb, innominate and lower limb, were recorded for adults. Age of epiphyseal closure was recorded for immature captive‐bornM. mulatta. Analysis of variance and principal component analyses tested significant differences between free‐range born and captive‐born individuals in each species. Significant differences were present in size and shape of postcrania between free‐range and captive‐born within taxa. Free‐range macaques were larger than captive‐born macaques, but this pattern did not consistently carry over to theSaguinussamples. Shape differences, while present throughout the skeleton, were especially prominent in the scapula. Differences in developmental timing, nutrition, and physical activity can be expected to contribute to the observed differences in postcranial skeletal form. These differences should be considered when captive‐born primates are included in morphological or evolutionary studies. Anat Rec, 2018. © 2018 Wiley Periodicals, Inc. Anat Rec, 302:761–774, 2019. © 2018 Wiley Periodicals, Inc.

 
more » « less
NSF-PAR ID:
10359843
Author(s) / Creator(s):
 ;  
Publisher / Repository:
Wiley Blackwell (John Wiley & Sons)
Date Published:
Journal Name:
The Anatomical Record
Volume:
302
Issue:
5
ISSN:
1932-8486
Page Range / eLocation ID:
p. 761-774
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Abstract Objectives

    The use of dental metrics in phylogenetic reconstructions of fossil primates assumes variation in tooth size is highly heritable. Quantitative genetic studies in humans and baboons have estimated high heritabilities for dental traits, providing a preliminary view of the variability of dental trait heritability in nonhuman primate species. To expand upon this view, the heritabilities and evolvabilities of linear dental dimensions are estimated in brown‐mantled tamarins (Saguinus fuscicollis) and rhesus macaques (Macaca mulatta).

    Materials and methods

    Quantitative genetic analyses were performed on linear dental dimensions collected from 302 brown‐mantled tamarins and 364 rhesus macaques. Heritabilities were estimated in SOLAR using pedigrees from each population, and evolvabilities were calculated manually.

    Results

    Tamarin heritability estimates range from 0.19 to 0.99, and 25 of 26 tamarin estimates are significantly different from zero. Macaque heritability estimates range from 0.08 to 1.00, and 25 out of 28 estimates are significantly different from zero.

    Discussion

    Dental dimensions are highly heritable in captive brown‐mantled tamarins and free‐ranging rhesus macaques. The range of heritability estimates in these populations is broadly similar to those of baboons and humans. Evolvability tends to increase with heritability, although evolvability is high relative to heritability in some dimensions. Estimating evolvability helps to contextualize differences in heritability, and the observed relationship between evolvability and heritability in dental dimensions requires further investigation.

     
    more » « less
  2. ABSTRACT

    Functional studies of skeletal anatomy are predicated on the fundamental assumption that form will follow function. For instance, previous studies have shown that the femora of specialized leaping primates are more robust than those of more generalized primate quadrupeds. Are such differences solely a plastic response to differential loading patterns during postnatal life, or might they also reflect more canalized developmental mechanisms present at birth? Here, we show that perinatalLemur catta, an arboreal/terrestrial quadruped, have less robust femora than perinatalPropithecus coquereli, a closely related species specialized for vertical clinging and leaping (a highly unusual locomotor mode in which the hindlimbs are used to launch the animal between vertical tree trunks). These results suggest that functional differences in long bone cross‐sectional dimensions are manifest at birth, belying simple interpretations of adult postcranial form as a direct record of loading patterns during postnatal life. Despite these significant differences in bone robusticity, we find that hindlimb bone mineralization, material properties, and measures of whole‐bone strength generally overlap in perinatalL. cattaandP. coquereli, indicating little differentiation in postcranial maturity at birth despite known differences in the pace of craniodental development between the species. In a broader perspective, our results likely reflect evolution acting during prenatal ontogeny. Even though primates are notable for relatively prolonged gestation and postnatal parental care, neonates are not buffered from selection, perhaps especially in the unpredictable and volatile environment of Madagascar. Anat Rec, 2018. © 2018 Wiley Periodicals, Inc. Anat Rec, 303:250–264, 2020. © 2018 American Association for Anatomy

     
    more » « less
  3. Abstract

    Taxonomic classification is important for understanding the natural world, yet current methods for species assessment often focus on craniodental morphology rather than the entire skeleton. Moreover, it is currently unknown how much variation could, or should, exist intragenerically. Here, we tested whether taxonomy can be accurately predicted based on patterns of morphological variation in macaques (H1) and whether postcranial bones reflect subgeneric macaque taxonomy similarly, or better, than the cranium (H2). Data included 3D scans of cranial and postcranial bones for eight macaque species (Macaca arctoides,Macaca fascicularis,Macaca fuscata,Macaca mulatta,Macaca nemestrina,Macaca nigra,Macaca radiata, andMacaca sylvanus). Fixed anatomical and semilandmarks were applied to scans of eight skeletal elements (crania = 45; mandible = 31; scapula = 66; humerus = 38; radius = 33; os coxa = 28; femur = 40; tibia = 40). For each skeletal element, regression analyses were performed to minimize the effects of sexual dimorphism. Between‐groups principal components analysis was used to visualize the major patterns of among‐species morphological variation, while the strength of correct taxon classification was measured with discriminant function analysis. Results suggested accepting the alternate hypothesis that different macaque species can be distinguished morphologically. Both cranial and many postcranial elements appeared to possess a taxonomic signal, and the limb bones—especially the upper limb—are reported to be more useful for taxonomic assessment than previously realized. Theoretically, certain behaviors and/or ecogeographical factors, as well as phylogeny, influenced skeletal morphology in macaques, likely contributing to taxonomic distinctions among different species.

     
    more » « less
  4. Taxonomic classification is fundamental for understanding the natural world, yet current methods for unknown species assessment are based on qualitative methods and focused on craniodental morphology. It is currently unknown how much variation could, or should, exist within a particular genus. Here, we tested whether taxonomy can be accurately predicted from patterns of morphological variation in a geographically widespread taxa, the macaques (H1) and whether postcranial bones reflect subgeneric taxonomy similarly, or better, than the cranium (H2). Data included 3D scans from nine species (M. arctoides, M. fascicularis, M. fuscata, M. mulatta, M. nemestrina, M. nigra, M. radiata, M. sylvanus, and outgroup Trachypithecus cristatus), for a sample of 297 individuals. Macaque species were chosen for their phylogenetic diversity and their geographic representation. 293 fixed and semilandmarks were applied to eight skeletal elements for each individual (crania=45; mandible=31; scapula=66; humerus=38; radius=33; os coxa=28; femur=40; tibia=40). A regression analysis was performed to minimize the effects of sexual dimorphism, making the primary input variables regression residuals. Patterns of variation were analyzed between- and within-species via Canonical Variates Analysis and 2D Multidimensional Scaling. Classificatory ability was tested using Discriminant Function Analysis. Results suggest that different species of macaque monkeys are taxonomically distinct and that the crania and postcrania possess a taxonomic signal. Some bones, like the limb bones, were more useful taxonomically than previously realized. Results suggest that taxonomic assessment should be updated to reflect newer methodologies and we argue that these results should inform future studies. 
    more » « less
  5. Abstract

    Primate craniofacial growth is traditionally assumed to cease upon maturation or at least be negligible, whereas bony remodeling is typically associated with advanced adult age and, in particular, tooth loss. Therefore, size and shape of the craniofacial skeleton of young and middle‐aged adults should be stable. However, research on both modern and historic human samples suggests that portions of theCFSexhibit age‐related changes in mature individuals, both related to and independent of tooth loss. These results demonstrate that the age‐category ‘adult’ is heterogeneous, containing individuals demonstrating post‐maturational age‐related variation, but the topic remains understudied outside of humans and in the cranial vault and base. Our research quantifies variation in a sample of captive adult female baboons (= 97) in an effort to understand how advancing age alters the matureCFS. Craniometric landmarks and sliding semilandmarks were collected fromcomputed tomography (CT)scans of adult baboons aged 7–32 years old. To determine whether craniofacial morphology is sensitive to aging mechanisms and whether any such effects are differentially distributed throughout the cranium, geometric morphometric techniques were employed to compare the shapes of various cranial regions among individuals of increasing age. Unexpectedly, the biggest form differences were observed between young and middle‐aged adults, rather than between adults with full dentitions and those with some degree of tooth loss. Shape variation was greatest in masticatory and nuchal musculature attachment areas. Our results indicate that thecraniofacial skeletonchanges form during adulthood in baboons, raising interesting questions about the molecular and biological mechanisms governing these changes.

     
    more » « less