Regional,ontogenetic, and sex‐related variations in elastic properties of cortical bone in baboon mandibles

Understanding the mechanical features of cortical bone and their changes with growth and adaptation to function plays an important role in our ability to interpret the morphology and evolution of craniofacial skeletons. We assessed the elastic properties of cortical bone of juvenile and adult baboon mandibles using ultrasonic techniques. Results showed that, overall, cortical bone from baboon mandibles could be modeled as an orthotropic elastic solid. There were significant differences in the directions of maximum stiffness, thickness, density, and elastic stiffness among different functional areas, indicating regional adaptations. After maturity, the cortical bone becomes thicker, denser, and stiffer, but less anisotropic. There were differences in elastic properties of the corpus and ramus between male and female mandibles which are not observed in human mandibles. There were correlations between cortical thicknesses and densities, between bone elastic properties and microstructural configuration, and between the directions of maximum stiffness and bone anatomical axes in some areas. The relationships between bone extrinsic and intrinsic properties bring us insights into the integration of form and function in craniofacial skeletons and suggest that we need to consider both macroscopic form, microstructural variation, and the material properties of bone matrix when studying the functional properties and adaptive nature of the craniofacial skeleton in primates. The differences between baboon and human mandibles is at variance to the pattern of differences in crania, suggesting differences in bone adaption to varying skeletal geometries and loading regimes at both phylogenetic and ontogenetic levels. Am J Phys Anthropol, 2010. © 2009 Wiley‐Liss, Inc.     

Elastic properties of external cortical bone in the craniofacial skeleton of the rhesus monkey

Knowledge of elastic properties and of their variation in the cortical bone of the craniofacial skeleton is indispensable for creating accurate finite-element models to explore the biomechanics and adaptation of the skull in primates. In this study, we measured elastic properties of the external cortex of the rhesus monkey craniofacial skeleton, using an ultrasonic technique. Twenty-eight cylindrical cortical specimens were removed from each of six craniofacial skeletons of adult Macaca mulatta. Thickness, density, and a set of longitudinal and transverse ultrasonic velocities were measured on each specimen to allow calculation of the elastic properties in three dimensions, according to equations derived from Newton's second law and Hooke's law. The axes of maximum stiffness were determined by fitting longitudinal velocities measured along the perimeter of each cortical specimen to a sinusoidal function. Results showed significant differences in elastic properties between different functional areas of the rhesus cranium, and that many sites have a consistent orientation of maximum stiffness among specimens. Overall, the cortical bones of the rhesus monkey skull can be modeled as orthotropic in many regions, and as transversely isotropic in some regions, e.g., the supraorbital region. There are differences from human crania, suggesting that structural differences in skeletal form relate to differences in cortical material properties across species. These differences also suggest that we require more comparative data on elastic properties in primate craniofacial skeletons to explore effectively the functional significance of these differences, especially when these differences are elucidated through modeling approaches, such as finite-element modeling.     

Cortical surface patterns in human and nonhuman primates

An analysis of skulls from several primate species shows that a “worm-track” surface pattern, first identified in the brow region in fossil adult hominids and subsequently in olive baboons, chimpanzees, and macaques, is also present in numerous other species. Fine cancellous bone and its attendant vermiculate surface pattern have been observed in subadult and adult gelada baboons, gibbons, gorillas, and orangutans as well as in modern Homo sapiens and several Plio-Pleistocene fossil hominids. In contemporary primates, fine cancellous bone has been identified not only in the brow region, but also along the zygomatic arch, on the pterygoid plates, on the maxilla, along the temporal line, on the mastoid process, and in the region of inion. Given the widespread distribution of this trait, caution is advised when using it as a diagnostic indicator of the evolutionary or functional significance of craniofacial morphology.     

Functional morphology of the asterionic region in extant hominoids and fossil hominids

Asterionic sutural patterns in Plio-Pleistocene hominid crania have never been examined in detail. We present an analysis of this anatomical region in Australopithecus and Homo and relate different sutural patterns to functional changes in the masticatory apparatus. The great apes and A. afarensis share the common adult higher primate sutural pattern referred to as the "asterionic notch," which develops in response to the hypertrophy of posterior temporalis muscle fibers and the consequent formation of compound temporal/nuchal crests. This sutural configuration also appears to be present on the early Homo cranium KNM-ER 1805. In contrast, adult male A. boisei crania exhibit a unique pattern where the temporal squama overlaps the parietal which, in turn, overlaps the par mastoidea and the upper scale of the occipital bone. We relate this arrangement to the need to reinforce the rear of a thin-walled braincase against the net tensile forces exerted by the temporalis and nuchal muscles. The common juvenile hominoid edge-to-edge asterionic articulation is maintained in adult A. africanus, A. robustus, female A. boisei, and most Homo crania. We discuss the latter pattern in regard to anterior temporalis hypertrophy in A. africanus, A. robustus, and A. boisei and to craniofacial paedomorphosis in Homo.     

Fatigue of immature baboon cortical bone

Strain-controlled uniaxial fatigue and monotonic tensile tests were conducted on turned femoral cortical bone specimens obtained from baboons at various ages of maturity. Fatigue loading produced a progressive loss in stiffness and an increase in hysteresis prior to failure, indicating that immature primate cortical bone responds to repeated loading in a fashion similar to that previously observed for adult human cortical bone. Bone fatigue resistance under this strain controlled testing decreased during maturation. Maturation was also associated with an increase in bone dry density, ash fraction and elastic modulus. The higher elastic modulus of more mature bone meant that these specimens were subjected to higher stress levels during testing than more immature bone specimens. Anatomical regions along the femoral shaft exhibited differences in strength and fatigue resistance.     

An Inquiry Safari: What Can We Learn From Skulls?

In this article, we describe an 8- to 10-day inquiry safari designed for middle/high school students to investigate hominid evolution using replica skulls of extant and extinct vertebrates. Students begin the unit using their own skulls and proceed to use the replica skulls of extant vertebrates to construct an understanding of how skulls can be used to interpret and infer diets, dentition, dental formulae, bipedal or quadrupedal locomotion, and the social structure of animals. They are then able to use this knowledge to construct similar inferences for extinct fossil hominids. Using radiometric dating data, the students develop possible phylogenetic pathways for hominid evolution. The lessons promote the use of inquiry skills including journaling, observing, drawing, puzzle-making, using taxonomic keys, and investigating into deep geological time.     

Accuracy of elastic property measurement in mandibular cortical bone is improved by using cylindrical specimens

Ultrasonic determination of elastic properties in human craniofacial cortical bone is problematic because of a lack of information about the principal material axes, and because the cortex is often thinner than in long bones. This study investigated solutions that permit reasonable determination of elastic properties in the human mandible. We tested whether ultrasonic velocities could be reliably measured in cylindrical samples of aluminum and mandibular bone, and the effects of reduced specimen thickness. Results indicted that (1) varying shape had minimal effects on ultrasonic velocities or derived elastic properties, and (2) ultrasonic velocities have relatively increased measurement error as propagation distances decreased. The increased error in velocity measurements of mandibular cortical specimens of less than 1.2 mm in thickness should be considered when assessing the reliability of single measurements.     

Hunting patterns and geographic profiling of white shark predation

Interspecific associations can arise for varied reasons including reduced predation risk and improved foraging success. In the case of bird–primate associations, birds typically appear to follow primate groups to harvest insects flushed by primates' movements. However, while previous studies have linked temporal changes in bird–primate associations to environmental conditions, few have assessed the additional effects of bird activity patterns and primate group behaviour and none have disentangled their potentially interdependent effects. Here, we test the hypothesis that foraging opportunities can drive interspecific associations in a previously undescribed bird–primate association between rock kestrels Falco rupicolus and chacma baboons Papio ursinus in central Namibia. Data were collected from two baboon groups and associated kestrels using instantaneous scan sampling during full-day follows over a 7-month field period, and analysed using generalized linear mixed models. We found that kestrel associations with baboons vary with season, show diurnal cycles and are more frequent when the baboons are in open desert habitat, engaged in travel foraging and in a large group. These patterns are statistically independent and consistent with the hypothesis that the kestrel–baboon association is driven by the foraging opportunities acquired by the kestrels. As the baboons do not appear to gain any benefits nor incur any costs from the association, we conclude that the kestrels are likely to be commensal with the baboons.     

Differences between the normal vaginal bacterial community of baboons and that of humans

Humans and baboons (Papio spp.) share considerable anatomical and physiological similarities in their reproductive tracts. Given the similarities, it is reasonable to expect that the normal vaginal microbial composition (microbiota) of baboons would be similar to that of humans. We have used a 16S rRNA phylogenetic approach to assess the composition of the baboon vaginal microbiota in a set of nine animals from a captive facility and six from the wild. Results show that although Gram‐positive bacteria dominate in baboons as they do in humans, there are major differences between the vaginal microbiota of baboons and that of humans. In contrast to humans, the species of Gram‐positive bacteria (Firmicutes) were taxa other than Lactobacillus species. In addition, some groups of Gram‐negative bacteria that are not normally abundant in humans were found in the baboon samples. A further level of difference was also seen even within the same bacterial phylogenetic group, as baboon strains tended to be more phylogenetically distinct from human strains than human strains were with each other. Finally, results of our analysis suggests that co‐evolution of microbes and their hosts cannot account for the major differences between the microbiota of baboons and that of humans because divergences between the major bacterial genera were too ancient to have occurred since primates evolved. Instead, the primate vaginal tracts appear to have acquired discrete subsets of bacteria from the vast diversity of bacteria available in the environment and established a community responsive to and compatible with host species physiology. Am. J. Primatol. 73:119–126, 2011. © 2010 Wiley‐Liss, Inc.     

Troop size and human-modified habitat affect the ranging patterns of a chacma baboon population in the cape peninsula, South Africa

Differences in group size and habitat use are frequently used to explain the extensive variability in ranging patterns found across the primate order. However, with few exceptions, our understanding of primate ranging patterns stems from studies of single groups and both intra- and inter-specific meta-analyses. Studies with many groups and those that incorporate whole populations are rare but important for testing socioecological theory in primates. We quantify the ranging patterns of nine chacma baboon troops in a single population and use Spearman rank correlations and generalized linear mixed models to analyze the effects of troop size and human-modified habitat (a proxy for good quality habitat) on home range size, density (individuals/km(2) ), and daily path length. Intrapopulation variation in home range sizes (1.5-37.7 km(2) ), densities (1.3-12.1 baboons/km(2) ), and daily path lengths (1.80-6.61 km) was so vast that values were comparable to those of baboons inhabiting the climatic extremes of their current distribution. Both troop size and human-modified habitat had an effect on ranging patterns. Larger troops had larger home ranges and longer daily path lengths, while troops that spent more time in human-modified habitat had shorter daily path lengths. We found no effect of human-modified habitat on home range size or density. These results held when we controlled for the effects of both a single large outlier troop living exclusively in human-modified habitat and baboon monitors on our spatial variables. Our findings confirm the ability of baboons, as behaviorally adaptable dietary generalists, to not only survive but also to thrive in human-modified habitats with adjustments to their ranging patterns in accordance with current theory. Our findings also caution that studies focused on only a small sample of groups within a population of adaptable and generalist primate species may underestimate the variability in their respective localities.     

Ontogeny and diachronic changes in sexual dimorphism in the craniofacial skeleton of rhesus macaques from Cayo Santiago, Puerto Rico

Insight into the ontogeny of sexual dimorphism is important to our understanding of life history, ecology, and evolution in primates. This study applied a three-dimensional method, Euclidean Distance Matrix Analysis, to investigate sexual dimorphism and its diachronic changes in rhesus macaque (Macaca mulatta) skulls. Twenty-one landmarks in four functional areas of the craniofacial skeleton were digitized from macaques of known age and sex from the Cayo Santiago collections. Then, a series of mean form matrices, form difference matrices, and growth matrices were computed to demonstrate growth curves, rates and duration of growth, and sexual dimorphism within the neurocranium, basicranium, palate, and face. The inclusion of fully adult animals revealed a full profile of sexual dimorphism. Additionally, we demonstrate for the first time diachronic change in adult sexual dimorphism caused by extended growth in adult females. A quicker growth rate in males from ages 2 to 8 was offset by a longer duration of growth in adult females that resulted in diminished dimorphism between the ages of 8 and 15. Four functional areas showed different sex-specific growth patterns, and the rate and duration of growth in the anterior facial skeleton contributed most to the changing profiles of sexual dimorphism. The late maturation in size of the female facial skeleton corresponds to later and less complete fusion of facial sutures. The prolongation of growth in females is hypothesized to be an evolutionary response to high levels of intrasexual competition, as is found in other primate species such as common chimpanzees with similar colony structure and reproductive behavior. Further investigation is required to determine (1) if this phenomenon observed in craniofacial skeletons is linked to sexual dimorphism in body size, and (2) whether this diachronic change in sexual dimorphism is species specific. The changing profile of sexual dimorphism in adult rhesus macaques suggests caution in studying sexual dimorphism in fossil primate and human forms.     

Scaling relationships between craniofacial sexual dimorphism and body mass dimorphism in primates: implications for the fossil record

Craniofacial remains (the most abundant identifiable remains in the fossil record) potentially offer important information about body size dimorphism in extinct species. This study evaluates the scaling relationships between body mass dimorphism and different measures of craniofacial dimorphism, evaluating taxonomic differences in the magnitude and scaling of craniofacial dimorphism across higher taxonomic groups. Data on 40 dimensions from 129 primate species and subspecies demonstrate that few dimensions change proportionally with body mass dimorphism. Primates show general patterns of greater facial vs. neurocranial and orbital dimorphism, and greater dimorphism in lengths as opposed to breadths. Within any species, though, different craniofacial dimensions can yield very different reconstructions of size dimorphism. There are significant taxonomic differences in the relationships between size and craniofacial dimorphism among primate groups that can have a significant impact on reconstructions of body mass dimorphism. Hominoids tend to show lower degrees of facial dimorphism proportional to size dimorphism than other primates. This in turn implies that strong craniofacial dimorphism in Australopithecus africanus could imply very strong body size dimorphism, conflicting with the relatively modest size dimorphism inferred from postcrania. Different methods of estimating the magnitude of size dimorphism from craniofacial measurements yield similar results, and yield comparatively low percent prediction errors for a number of dimensions. However, confidence intervals for most estimates are so large as to render most estimates highly tentative.     

Survival and reproduction in the first two years following a large-scale primate colony move and social reorganization

(Macaca nemestrina) and baboon (Papio cynocephalus, Papio anubis, and hybrids) breeding colonies from the Primate Field Station (PFS) (Medical Lake, WA) to the Tulane Regional Primate Research Center (Covington, LA). Colony records on all 598 pigtailed macaques (Macaca nemestrina) and 157 baboons (P. c. anubis) shipped to the Tulane Primate Center from the PFS breeding colony were used for analysis of species, sex, age, origin, current status, and the number of animals born at Tulane and their status. To provide comparative statistics, colony records on all 1,002 macaques and 258 baboons alive on 1 January 1991 at the Field Station were retrieved in the same manner as the Tulane data. Overall survival rates of macaques in the months following the move (71.7%) were similar to those associated with the Arashiyama West colony move from Japan to Texas. In our colony, significantly lower survival following the move was seen only in older (10 years+) macaques, while survival in other age groups was slightly lower than in the comparison year of 1991 at the Primate Field Station. Captive-bred macaques exhibited higher survival than wild-caught animals. Infant survival at Tulane was not significantly different than in pre-move years. Baboons fared well in the move, with no significant differences in mortality or reproduction when compared with the 1991 Medical Lake baboon colony.     

Interspecies transmission of macaque simian T-cell leukemia/lymphoma virus type 1 in baboons resulted in an outbreak of malignant lymphoma.

An outbreak of malignant lymphoma has been observed in one of the baboon (Papio hamadryas) stocks of Sukhumi Primate Center. More than 300 cases in this "high-lymphoma stock" have been registered since 1967. Human T-cell lymphotropic virus type 1 (HTLV-1)-related virus was implicated as the etiologic agent of Sukhumi baboon lymphoma. The origin of this virus remained unclear. Two possibilities were originally considered: the origin could be baboon simian T-cell leukemia/lymphoma virus type 1 (STLV-1) or HTLV-1 (before the outbreak started, some Sukhumi baboons were inoculated with human leukemic material). The third possibility entered recently: interspecies transmission of rhesus macaque STLV-1 to baboons. It was prompted by the finding of very close similarity between STLV-1 991-1cc (the strain isolated from a non-Sukhumi baboon inoculated with material from a Sukhumi lymphomatous baboon) and rhesus STLV-1. To test this hypothesis, we investigated 37 Sukhumi STLV-1 isolates from baboons of high-lymphoma stock by PCR discriminating rhesus type and baboon type STLV-1 isolates. All of them were proved to be rhesus type STLV-1. In contrast, all six STLV-1 isolates from baboons belonging to other stocks or populations were of baboon type. The PCR results were fully confirmed by DNA sequence data. The partial env gene gene sequences of all four STLV-1 isolates from Sukhumi lymphomatous baboons were 97 to 100% similar to the sequence of known rhesus STLV-1 and only 85% homologous with the sequence of conventional baboon STLV-1. Thus, interspecies transmission of STLV-1 from rhesus macaques (or closely related species) to baboons occurred at Sukhumi Primate Center. Most probably this event initiated the outbreak of lymphoma in Sukhumi baboons.     

Ontogeny of limb mass distribution in infant baboons (Papio cynocephalus)

Primates have more distally distributed limb muscle mass compared to most nonprimate mammals. The heavy distal limbs of primates are likely related to their strong manual and pedal grasping abilities, and interspecific differences in limb mass distributions among primates are correlated with the amount of time spent on arboreal supports. Within primate species, individuals at different developmental stages appear to differ in limb mass distribution patterns. For example infant macaques have more distally distributed limb mass at young ages. A shift from distal to proximal limb mass concentrations coincides with a shift from dependent travel (grasping their mother's hair) to independent locomotion. Because the functional demands placed on limbs may differ between taxa, understanding the ontogeny of limb mass distribution patterns is likely an essential element in interpreting the diversity of limb mass distribution patterns present in adult primates. This study examines changes in limb inertial properties during ontogeny in a longitudinal sample of infant baboons (Papio cynocephalus). The results of this study show that infant baboons undergo a transition from distal to proximal limb mass distribution patterns. This transition in limb mass distribution coincides with the transition from dependent to independent locomotion during infant development. Compared to more arboreal macaques, infant baboons undergo a faster transition to more proximal limb mass distribution patterns. These results suggest that functional demands placed on the limbs during ontogeny have a strong impact on the development of limb mass distribution patterns.     

Baboon immunoglobulin constant region heavy chains: identification of four <Emphasis Type="Italic">IGHG</Emphasis> genes

The increasing use of nonhuman primate models in biomedical research and especially in vaccine development requires the characterization of their immunoglobulin genes and corresponding products. Therefore, we sequenced, cloned and characterized the four immunoglobulin gamma chain constant region genes ( IGHG) present in baboons. These four genes were designated IGHG1, IGHG2, IGHG3 and IGHG4 on the basis of sequence similarities with the four human genes encoding the IgG1, IgG2, IgG3 and IgG4 subclasses and the three known rhesus macaque IGHG genes. Specifically, the baboon IgG1, IgG2, IgG3 and IgG4 sequences exhibit 90.3%, 88.3%, 86.7% and 89.6% amino acid identity to their human counterpart. The percent of amino acid identity of baboon IgG1, IgG2 and IgG3 to the corresponding rhesus macaque sequences is 98.5, 93.1 and 94.4, respectively. Therefore, baboon and rhesus macaque IGHG genes are highly homologous to each other. The majority of differences existing between baboon and human sequences are clustered in the hinge region, with the upper hinge being the most diverse and containing several proline residues. Similar to rhesus macaques, the hinge regions of all baboon IGHG genes consist of a single exon, whereas in humans the IgG3 molecule is encoded by multiple exons. These results confirm the evolutionary instability of the hinge region and indicate that functional properties associated with the hinge regions of baboon and human IgG molecules might differ between the two species.     

Effects of age and gender on the location and orientation of the foramen magnum in rhesus macaques (Macaca mulatta)

Endocasts from 378 rhesus macaque skulls from the Cayo Santiago skeletal collection were measured to determine the effects of age and gender on the position and orientation of the foramen magnum. The foramen magnum migrates from a rostral to a caudal position and its angle changes during postnatal development. The angles and relative positions of the foramen magnum are similar for both genders of infants and for both genders of adults. However, analyses of linear response and plateau (LRP) functions reveal significant differences between males and females in the timing of reorientation of the angle and migration of the foramen magnum. The mean adult angle and relative position of the foramen magnum are reached by 4.7 years in females, but they do not achieve their adult values until 7.1 years in males. A similar pattern is observed for the brainstem region of the basicranium. Mean adult lengths of the brainstem region are reached at 5.2 years in females and 7.1 years in males. The relationships between cranial capacity, the growth pattern of the brainstem, and the pattern of change for the angle and the relative position of the foramen magnum are examined. Quantification of the effects of age and gender on the location of the foramen magnum in a large sample of endocasts from one species of higher primate has potential implications for research on human development, and for interpretation of juvenile specimens in the hominid fossil record.     

Growth changes in internal and craniofacial flexion measurements.

Growth changes in both internal and craniofacial flexion angles are presented for Pan troglodytes, Gorilla gorilla, and modern humans. The internal flexion angle (IFA) was measured from lateral radiographs, and the craniofacial flexion angle (CFA) was calculated from coordinate data. Stage of dental development is used as a baseline for examination of growth changes and nonparametric correlations between flexion angles and dental development stage are tested for significance. In Gorilla, the IFA increases during growth. The IFA is relatively stable in Pan and modern humans. Pan and Gorilla display an increase in the CFA. However, this angle decreases during growth in modern humans. Flexion angles were derived from coordinate data collected for several early hominid crania. Measurements for two robust australopithecine crania indicate strong internal flexion. It has been suggested that cerebellar expansion in this group may relate to derived features of the posterior cranial base. In general, australopithecine crania exhibit craniofacial flexion intermediate between great apes and modern humans. The "archaic" Homo sapiens specimen from Kabwe is most similar to modern humans.     

Cortical Folding of the Primate Brain: An Interdisciplinary Examination of the Genetic Architecture,Modularity, and Evolvability of a Significant Neurological Trait in Pedigreed Baboons (Genus Papio)

Folding of the primate brain cortex allows for improved neural processing power by increasing cortical surface area for the allocation of neurons. The arrangement of folds (sulci) and ridges (gyri) across the cerebral cortex is thought to reflect the underlying neural network. Gyrification, an adaptive trait with a unique evolutionary history, is affected by genetic factors different from those affecting brain volume. Using a large pedigreed population of ∼1000 Papio baboons, we address critical questions about the genetic architecture of primate brain folding, the interplay between genetics, brain anatomy, development, patterns of cortical–cortical connectivity, and gyrification’s potential for future evolution. Through Mantel testing and cluster analyses, we find that the baboon cortex is quite evolvable, with high integration between the genotype and phenotype. We further find significantly similar partitioning of variation between cortical development, anatomy, and connectivity, supporting the predictions of tension-based models for sulcal development. We identify a significant, moderate degree of genetic control over variation in sulcal length, with gyrus-shape features being more susceptible to environmental effects. Finally, through QTL mapping, we identify novel chromosomal regions affecting variation in brain folding. The most significant QTL contain compelling candidate genes, including gene clusters associated with Williams and Down syndromes. The QTL distribution suggests a complex genetic architecture for gyrification with both polygeny and pleiotropy. Our results provide a solid preliminary characterization of the genetic basis of primate brain folding, a unique and biomedically relevant phenotype with significant implications in primate brain evolution.