Body composition in Pan paniscus compared with Homo sapiens has implications for changes during human evolution.

The human body has been shaped by natural selection during the past 4-5 million years. Fossils preserve bones and teeth but lack muscle, skin, fat, and organs. To understand the evolution of the human form, information about both soft and hard tissues of our ancestors is needed. Our closest living relatives of the genus Pan provide the best comparative model to those ancestors. Here, we present data on the body composition of 13 bonobos (Pan paniscus) measured during anatomical dissections and compare the data with Homo sapiens. These comparative data suggest that both females and males (i) increased body fat, (ii) decreased relative muscle mass, (iii) redistributed muscle mass to lower limbs, and (iv) decreased relative mass of skin during human evolution. Comparison of soft tissues between Pan and Homo provides new insights into the function and evolution of body composition.

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.

Ontogenetic scaling of fore limb and hind limb joint posture and limb bone cross-sectional geometry in vervets and baboons.

OBJECTIVES: Previous studies suggest that the postures habitually adopted by an animal influence the mechanical loading of its long bones. Relatively extended limb postures in larger animals should preferentially reduce anteroposterior (A-P) relative to mediolateral (M-L) bending of the limb bones and therefore decrease A-P/M-L rigidity. We test this hypothesis by examining growth-related changes in limb bone structure in two primate taxa that differ in ontogenetic patterns of joint posture. MATERIALS AND METHODS: Knee and elbow angles of adult and immature vervets (Chlorocebus aethiops, n = 16) were compared to published data for baboons (Papio hamadryas ursinus, n = 33, Patel et al., ). Ontogenetic changes in ratios of A-P/M-L bending rigidity in the femur and humerus were compared in skeletal samples (C. aethiops, n = 28; P. cynocephalus, n = 39). Size changes were assessed with linear regression, and age group differences tested with ANOVA. RESULTS: Only the knee of baboons shows significant postural change, becoming more extended with age and mass. A-P/M-L bending rigidity of the femur decreases during ontogeny in immature and adult female baboons only. Trends in the humerus are less marked. Adult male baboons have higher A-P/M-L bending rigidity of the femur than females. CONCLUSIONS: The hypothesized relationship between more extended joints and reduced A-P/M-L bending rigidity is supported by our results for immature and adult female baboon hind limbs, and the lack of significant age changes in either parameter in forelimbs and vervets. Adult males of both species depart from general ontogenetic trends, possibly due to socially mediated behavioral differences between sexes. Am J Phys Anthropol 161:72-83, 2016. © 2016 Wiley Periodicals, Inc.

The real females of human evolution.

When "woman-the-gatherer" was first proposed as a counter to "man-the-hunter," we were only beginning to understand the many faces of primate females. In ensuing decades we have learned about the skills and talents of female chimpanzees in tool using, hunting, and transmitting behaviors from one generation to the next as teachers, and across space as newcomers to neighboring communities. The perspective of evolutionary time highlights the continuity of female lives from the origin of mammals to the origin of Homo sapiens. The combination of behavioral, fossil, and archeological information aid in reconstructing key ingredients acquired by females along the way that contributed to the success of our species.

Skeletal development in Pan paniscus with comparisons to Pan troglodytes.

Fusion of skeletal elements provides markers for timing of growth and is one component of a chimpanzee's physical development. Epiphyseal closure defines bone growth and signals a mature skeleton. Most of what we know about timing of development in chimpanzees derives from dental studies on Pan troglodytes. Much less is known about the sister species, Pan paniscus, with few in captivity and a wild range restricted to central Africa. Here, we report on the timing of skeletal fusion for female captive P. paniscus (n = 5) whose known ages range from 0.83 to age 11.68 years. Observations on the skeletons were made after the individuals were dissected and bones cleaned. Comparisons with 10 female captive P. troglodytes confirm a generally uniform pattern in the sequence of skeletal fusion in the two captive species. We also compared the P. paniscus to a sample of three unknown-aged female wild P. paniscus, and 10 female wild P. troglodytes of known age from the Taï National Park, Côte d'Ivoire. The sequence of teeth emergence to bone fusion is generally consistent between the two species, with slight variations in late juvenile and subadult stages. The direct-age comparisons show that skeletal growth in captive P. paniscus is accelerated compared with both captive and wild P. troglodytes populations. The skeletal data combined with dental stages have implications for estimating the life stage of immature skeletal materials of wild P. paniscus and for more broadly comparing the skeletal growth rates among captive and wild chimpanzees (Pan), Homo sapiens, and fossil hominins.

Brief communication: dental development timing in captive Pan paniscus with comparisons to Pan troglodytes.

Dental eruption provides markers of growth and is one component of a chimpanzee's physical development. Dental markers help characterize transitions between life stages, e.g., infant to juvenile. Most of what we know about the timing of development in chimpanzees derives from Pan troglodytes. Much less is known about the sister species, Pan paniscus, with few in captivity and a restricted wild range in central Africa. Here we report on the dental eruption timing for female captive P. paniscus (n = 5) from the Milwaukee and San Diego Zoos whose ages are known and range from birth to age 8.54 years. Some observations were recorded in zoo records on the gingiva during life; others were made at death on the gingiva and on the skeleton. At birth, P. paniscus infants have no teeth emerged. By 0.83 years, all but the deciduous second molars (dm(2) ) (when both upper and lower dentitions are referenced collectively, no super or subscript notation is used) and canines (dc) are emerged. For permanent teeth, results show a sequence polymorphism for an early P4 eruption, not previously described for P. paniscus. Comparisons between P. paniscus and P. troglodytes document absolute timing differences of emergence in upper second incisors (I(2) ), and upper and lower canines (C) and third molars (M3). The genus Pan encompasses variability in growth not previously recognized. These preliminary data suggest that physical growth in captive P. paniscus may be accelerated, a general pattern found in captive P. troglodytes.

Stable carbon and nitrogen isotope enrichment in primate tissues.

Isotopic studies of wild primates have used a wide range of tissues to infer diet and model the foraging ecologies of extinct species. The use of mismatched tissues for such comparisons can be problematic because differences in amino acid compositions can lead to small isotopic differences between tissues. Additionally, physiological and dietary differences among primate species could lead to variable offsets between apatite carbonate and collagen. To improve our understanding of the isotopic chemistry of primates, we explored the apparent enrichment (ε*) between bone collagen and muscle, collagen and fur or hair keratin, muscle and keratin, and collagen and bone carbonate across the primate order. We found that the mean ε* values of proteinaceous tissues were small (≤1‰), and uncorrelated with body size or phylogenetic relatedness. Additionally, ε* values did not vary by habitat, sex, age, or manner of death. The mean ε* value between bone carbonate and collagen (5.6 ± 1.2‰) was consistent with values reported for omnivorous mammals consuming monoisotopic diets. These primate-specific apparent enrichment values will be a valuable tool for cross-species comparisons. Additionally, they will facilitate dietary comparisons between living and fossil primates.

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.

Morphological variation in adult chimpanzees (Pan troglodytes verus) of the Taï National Park, Côte d'Ivoire.

Twenty five adult chimpanzee skeletons (Pan troglodytes verus) of known age and sex (15 females, 10 males) from a long-term study site in Taï National Park, Cote d'Ivoire present new data on variation. These skeletons provide a rare opportunity to measure the cranium and postcranium from the same individuals. We compare measurements and indices of the Taï sample with those of relatively complete Pan troglodytes schweinfurthii skeletons from Gombe National Park, Tanzania. Measurements of Pan paniscus are included as an outside comparison. The Taï and Gombe samples are analyzed by sex; combined sex samples are compared between the two groups, and the two sexes to each other. Taï females and males do not differ in most long bone lengths or in pelvic dimensions, but do differ significantly in cranial capacity, facial measurements, clavicle length, scapular breadth, and femur length. Gombe females and males differ significantly in some facial measurements and in scapular breadth. In combined sex samples, Taï individuals have lower cranial capacity, longer palate and mandible, and greater dimensions in the trunk and limb lengths. Taï females account for most of the variation; males differ from each other only in greater length of humerus and femur. The Taï skeletons provide new data for assessing individual variation and sexual dimorphism within and between populations and species. The combination of cranial and postcranial data provides a clearer picture of chimpanzee intraspecific and interspecific variation than can be gained from either data set alone.

Locomotor Anatomy and Behavior of Patas Monkeys (Erythrocebus patas) with Comparison to Vervet Monkeys (Cercopithecus aethiops).

Patas monkeys (Erythrocebus patas) living in African savanna woodlands and grassland habitats have a locomotor system that allows them to run fast, presumably to avoid predators. Long fore- and hindlimbs, long foot bones, short toes, and a digitigrade foot posture were proposed as anatomical correlates with speed. In addition to skeletal proportions, soft tissue and whole body proportions are important components of the locomotor system. To further distinguish patas anatomy from other Old World monkeys, a comparative study based on dissection of skin, muscle, and bone from complete individuals of patas and vervet monkeys (Cercopithecus aethiops) was undertaken. Analysis reveals that small adjustments in patas skeletal proportions, relative mass of limbs and tail, and specific muscle groups promote efficient sagittal limb motion. The ability to run fast is based on a locomotor system adapted for long distance walking. The patas' larger home range and longer daily range than those of vervets give them access to highly dispersed, nutritious foods, water, and sleeping trees. Furthermore, patas monkeys have physiological adaptations that enable them to tolerate and dissipate heat. These features all contribute to the distinct adaptation that is the patas monkeys' basis for survival in grassland and savanna woodland areas.

Anatomical Contributions to Hylobatid Taxonomy and Adaptation.

Compared with the great apes, the small-bodied hylobatids were treated historically as a relatively uniform group with 2 genera, Hylobates and the larger-bodied Symphalangus. Four genera are now recognized, each with a different chromosome number: Hoolock (hoolock) (38), Hylobates (44), Nomascus (crested gibbon) (52), and Symphalangus (siamang) (50). Previous morphological studies based on relative bone lengths, e.g., intermembral indices; molar tooth sizes; and body masses did not distinguish the 4 genera from each other. We applied quantitative anatomical methods to test the hypothesis that each genus can be differentiated from the others using the relative distribution of body mass to the forelimbs and hind limbs. Based on dissections of 13 hylobatids from captive facilities, our findings demonstrate that each of the 4 genera has a distinct pattern of body mass distribution. For example, the adult Hoolock has limb proportions of nearly equal mass, a pattern that differentiates it from species in the genus Hylobates, e.g., H. lar (lar gibbon), H. moloch (Javan gibbon), H. pileatus (pileated gibbon), Nomascus, and Symphalangus. Hylobates is distinct in having heavy hind limbs. Although Symphalangus has been treated as a scaled up version of Hylobates, its forelimb exceeds its hind limb mass, an unusual primate pattern otherwise found only in orangutans. This research provides new information on whole body anatomy and adds to the genetic, ecological, and behavioral evidence for clarifying the taxonomy of the hylobatids. The research also underscores the important contribution of studies on rare species in captivity.

Functional anatomy and adaptation of male gorillas (Gorilla gorilla gorilla) with comparison to male orangutans (Pongo pygmaeus).

Great apes diversified during the Miocene in Old World forests. Two lineages, gorillas in Africa and orangutans in Asia, have sexual dimorphisms of super-sized males, though they presumably diverged from a smaller common ancestor. We test the hypothesis that they increased in body mass independently and convergently, and that their many postcranial differences reflect locomotor differences. Whole body dissections of five adult male gorillas and four adult male orangutans allowed quantification of body mass distribution to limb segments, of body composition (muscle, bone, skin, and fat relative to total body mass), and of muscle distribution and proportions. Results demonstrate that gorilla forelimb anatomy accommodates shoulder joint mobility for vertical climbing and reaching while maintaining joint stability during quadrupedal locomotion. The heavily muscled hind limbs are equipped for propulsion and weight-bearing over relatively stable substrates on the forest floor. In contrast, orangutan forelimb length, muscle mass, and joint construction are modified for strength and mobility in climbing, bridging, and traveling over flexible supports through the forest canopy. Muscles of hip, knee, and ankle joints provide rotational and prehensile strength essential for moving on unstable and discontinuous branches. We conclude that anatomical similarities are due to common ancestry and that differences in postcranial anatomy reflect powerful selection for divergent locomotor adaptations. These data further support the evolutionary conclusion that gorillas fall with chimpanzees and humans as part of the African hominoid radiation; orangutans are a specialized outlier.