Primary bone microanatomy records developmental aspects of life history in catarrhine primates.

A central challenge in human origins research is to understand how evolution has shaped modern human life history. As fossilized remains of our ancestors provide the only direct evidence for life history evolution, efforts to reconstruct life history in paleontological contexts have focused on hard tissues, particularly on dental development. However, among investigators of other vertebrate groups, there is a long tradition of examining primary bone microstructure to decipher growth rates and maturational timing, based on an empirical relationship between the microanatomy of primary bone and the rate at which it is deposited. We examined ontogenetic variation in primary bone microstructure at the midshaft femur of Chlorocebus aethiops, Hylobates lar, and Pan troglodytes to test whether tissue type proportions vary in accordance with predictions based on body mass growth patterns described previously. In all taxa, younger age classes were characterized by significantly higher percent areas of fibro-lamellar and/or parallel-fibered tissues, while older age classes showed significantly higher proportions of lamellar bone. In prior experimental studies, fibro-lamellar and parallel-fibered tissue types have been associated with faster depositional rates than lamellar bone. Principal components analysis revealed differences among taxa in the timing of this transition, and in the particular tissue types observed among individuals of similar dental emergence status. Among M1 and M2 age classes, higher proportions of parallel-fibered and fibro-lamellar tissues were observed in those taxa characterized by reportedly faster body mass growth rates. Further, persistence of fibro-lamellar tissue throughout DECID, M1 and M2 age classes in chimpanzees contrasts with the pattern reported previously for modern humans. Despite the necessary limitations of our cross-sectional study design and the secondary remodeling of bone in primates, large areas of primary bone remain intact and represent a valuable and independent source of information about the evolution of growth and development in the fossil record.

Growth and the development of sexual size dimorphism in lorises and galagos.

Three fundamental ontogenetic pathways lead to the development of size differences between males and females. Males and females may grow at the same rate for different durations (bimaturism), grow for the same duration at different rates, or grow at a mix of rate and duration differences. While patterns of growth and the development of adult body size are well established for many haplorhines, the extent to which rate and duration differences affect strepsirrhine growth trajectories remains unclear. Here, we present iterative piecewise regression models that describe the ontogeny of adult body mass for males and females of five lorisoid species (i.e., lorises and galagos) from the Duke Lemur Center. We test the hypotheses that, like most haplorhines, sexual size dimorphism (SSD) is a result of bimaturism, and males and females of monomorphic species grow at the same rate for a similar duration. We confirm that the galagos in this sample (Galago moholi and Otolemur garnettii) show significant SSD that is achieved through bimaturism. Unlike monomorphic lemurids, the lorises in this sample show a diversity of ontogenetic patterns. Loris tardigradus does follow a lemur-like trajectory to monomorphism but Nycticebuscoucang and Nycticebus pygmaeus achieve larger adult female body sizes through a mixture of rate and duration differences. We show that contrary to previous assumptions, there are patterns of both similarity and difference in growth trajectories of comparably sized lorises and galagos. Furthermore, when ontogenetic profiles of lorisoid and lemurid growth are compared, it is evident that lorisoids grow faster for a shorter period of time.

Muscle mass scaling in primates: an energetic and ecological perspective.

Body composition is known to vary dramatically among mammals, even in closely related species, yet this issue has never been systematically investigated. Here, we examine differences in muscle mass scaling among mammals, and explore how primate body composition compares to that of nonprimate mammals. We use a literature-based sample of eutherian and metatherian mammals, and combine this with new dissection-based data on muscularity in a variety of strepsirrhine primates and the haplorhine, Tarsius syrichta. Our results indicate an isometric scaling relationship between total muscle mass and total body mass across mammals. However, we documented substantial variation in muscularity in mammals (21-61% of total body mass), which can be seen both within and between taxonomic groups. We also found that primates are under-muscled when compared to other mammals. This difference in body composition may in part reflect the functional consequences of arboreality, as arboreal species have significantly lower levels of muscularity than terrestrial species.

The effects of core suture purchase on the biomechanical characteristics of a multistrand locking flexor tendon repair: a cadaveric study.

PURPOSE: To determine the effects of suture purchase on work of flexion (WOF), 2-mm gap force, and load to failure on the combination cross-locked cruciate-interlocking horizontal mattress (CLC-IHM) flexor tendon repair in zone II. METHODS: A total of 33 fresh-frozen cadaveric fingers were mounted in a custom jig, and the flexor digitorum profundus of each finger was fixed to the mobile arm of a tensile strength machine. Initial measurements of WOF were obtained. Each tendon was repaired with the CLC core suture, randomly assigned to placement of 3, 5, 7 or 10 mm from the cut edge of the tendon, and completed with the IHM circumferential suture. After the repair was completed, measurements of WOF were repeated. Each finger was cycled 1000 times. After each 250 cycles, gapping was recorded, and WOF was measured again. Change in WOF (WOF after repair - WOF of intact tendon) was calculated. Tendons were then dissected from the fingers and linearly tested for 2-mm gap force and ultimate load to failure. RESULTS: The group repaired at 10 mm had the lowest percent increase in WOF (5.2%), the highest 2-mm gap force (89.8 N), and the highest ultimate load to failure (111.5 N). The group repaired at 3 mm had the highest percent increase in WOF (22.1%), the lowest 2-mm gap force (54.6 N), and the lowest ultimate load to failure (84.6 N). CONCLUSIONS: A 10-mm suture purchase is the recommended distance for optimal performance for the CLC-IHM combination repair method. This method with a 10-mm suture purchase has a low increase in WOF, high strength, and high resistance to gapping, and it should be strong enough to tolerate early motion.

Regional variability in secondary remodeling within long bone cortices of catarrhine primates: the influence of bone growth history.

Secondary intracortical remodeling of bone varies considerably among and within vertebrate skeletons. Although prior research has shed important light on its biomechanical significance, factors accounting for this variability remain poorly understood. We examined regional patterning of secondary osteonal bone in an ontogenetic series of wild-collected primates, at the midshaft femur and humerus of Chlorocebus (Cercopithecus) aethiops (n = 32) and Hylobates lar (n = 28), and the midshaft femur of Pan troglodytes (n = 12). Our major objectives were: 1) to determine whether secondary osteonal bone exhibits significant regional patterning across inner, mid-cortical and outer circumferential cortical rings within cross-sections; and if so, 2) to consider the manner in which this regional patterning may reflect the influence of relative tissue age and other circumstances of bone growth. Using same field-of-view images of 100-microm-thick cross-sections acquired in brightfield and circularly polarized light microscopy, we quantified the percent area of secondary osteonal bone (%HAV) for whole cross-sections and across the three circumferential rings within cross-sections. We expected bone areas with inner and middle rings to exhibit higher %HAV than the outer cortical ring within cross-sections, the latter comprising tissues of more recent depositional history. Observations of primary bone microstructural development provided an additional context in which to evaluate regional patterning of intracortical remodeling. Results demonstrated significant regional variability in %HAV within all skeletal sites. As predicted,%HAV was usually lowest in the outer cortical ring within cross-sections. However, regional patterning across inner vs. mid-cortical rings showed a more variable pattern across taxa, age classes, and skeletal sites examined. Observations of primary bone microstructure revealed that the distribution of endosteally deposited bone had an important influence on the patterning of secondary osteonal bone across rings. Further, when present, endosteal compacted coarse cancellous bone always exhibited some evidence of intracortical remodeling, even in those skeletal sites exhibiting comparatively low %HAV overall. These results suggest that future studies should consider the local developmental origin of bone regions undergoing secondary remodeling later in life, for an improved understanding of the manner in which developmental and mechanical factors may interact to produce the taxonomic and intraskeletal patterning of secondary bone remodelling in adults.

Collagen Fiber Orientation in Primate Long Bones.

Studies of variation in orientation of collagen fibers within bone have lead to the proposition that these are preferentially aligned to accommodate different kinds of load, with tension best resisted by fibers aligned longitudinally relative to the load, and compression best resisted by transversely aligned fibers. However, previous studies have often neglected to consider the effect of developmental processes, including constraints on collagen fiber orientation (CFO), particularly in primary bone. Here we use circularly polarized light microscopy to examine patterns of CFO in cross-sections from the midshaft femur, humerus, tibia, radius, and ulna in a range of living primate taxa with varied body sizes, phylogenetic relationships and positional behaviors. We find that a preponderance of longitudinally oriented collagen is characteristic of both periosteal primary and intracortically remodeled bone. Where variation does occur among groups, it is not simply understood via interpretations of mechanical loads, although prioritized adaptations to tension and/or shear are considered. While there is some suggestion that CFO may correlate with body size, this relationship is neither consistent nor easily explicable through consideration of size-related changes in mechanical adaptation. The results of our study indicate that there is no clear relationship between CFO and phylogenetic status. One of the principle factors accounting for the range of variation that does exist is primary tissue type, where slower depositing bone is more likely to comprise a larger proportion of oblique to transverse collagen fibers. Anat Rec, 300:1189-1207, 2017. © 2017 Wiley Periodicals, Inc.

Interindividual variation in functionally adapted trait sets is established during postnatal growth and predictable based on bone robustness.

Adults acquire unique sets of morphological and tissue-quality bone traits that are predictable based on robustness and deterministic of strength and fragility. How and when individual trait sets arise during growth has not been established. Longitudinal structural changes of the metacarpal diaphysis were measured for boys and girls from 3 mo to 8 yr of age using hand radiographs obtained from the Bolton-Brush collection. Robustness varied approximately 2-fold among boys and girls, and individual values were established by 2 yr of age, indicating that genetic and environmental factors controlling the relationship between growth in width and growth in length were established early during postnatal growth. Significant negative correlations between robustness and relative cortical area and a significant positive correlation between robustness and a novel measure capturing the efficiency of growth indicated that coordination of the subperiosteal and endocortical surfaces was responsible for this population acquiring a narrow range of trait sets that was predictable based on robustness. Boys and girls with robust diaphyses had proportionally thinner cortices to minimize mass, whereas children with slender diaphyses had proportionally thicker cortices to maximize stiffness. Girls had more slender metacarpals with proportionally thicker cortices compared with boys at all prepubertal ages. Although postnatal growth patterns varied in fundamentally different ways with sex and robustness, the dependence of trait sets on robustness indicated that children sustained variants affecting subperiosteal growth because they shared a common biological factor regulating functional adaptation. Considering the natural variation in acquired trait sets may help identify determinants of fracture risk, because age-related bone loss and gain will affect slender and robust structures differently.

Genetic randomization reveals functional relationships among morphologic and tissue-quality traits that contribute to bone strength and fragility.

We examined femora from adult AXB/BXA recombinant inbred (RI) mouse strains to identify skeletal traits that are functionally related and to determine how functional interactions among these traits contribute to genetic variability in whole-bone stiffness, strength, and toughness. Randomization of A/J and C57BL/6J genomic regions resulted in each adult male and female RI strain building mechanically functional femora by assembling unique sets of morphologic and tissue-quality traits. A correlation analysis was conducted using the mean trait values for each RI strain. A third of the 66 correlations examined were significant, indicating that many bone traits covaried or were functionally related. Path analysis revealed important functional interactions among bone slenderness, cortical thickness, and tissue mineral density. The path coefficients describing these functional relations were similar for both sexes. The causal relationship among these three traits suggested that cellular processes during growth simultaneously regulate bone slenderness, cortical thickness, and tissue mineral density so that the combination of traits is sufficiently stiff and strong to satisfy daily loading demands. A disadvantage of these functional interactions was that increases in tissue mineral density also deleteriously affected tissue ductility. Consequently, slender bones with high mineral density may be stiff and strong but they are also brittle. Thus, genetically randomized mouse strains revealed a basic biological paradigm that allows for flexibility in building bones that are functional for daily activities but that creates preferred sets of traits under extreme loading conditions. Genetic or environmental perturbations that alter these functional interactions during growth would be expected to lead to loss of function and suboptimal adult bone quality.