Body proportions and environmental adaptation in gorillas.

OBJECTIVES: Limb length and trunk proportions are determined in a large, taxonomically and environmentally diverse sample of gorillas and related to variation in locomotion, climate, altitude, and diet. MATERIALS AND METHODS: The sample includes 299 gorilla skeletons, 115 of which are infants and juveniles, distributed between western lowland (G. gorilla gorilla), low and high elevation grauer (G. beringei graueri), and Virunga mountain gorillas (G. b. beringei). Limb bone and vertebral column lengths scaled to body mass are compared between subgroups by age group. RESULTS: All G. beringei have relatively short 3rd metapodials and manual proximal phalanges compared to G. gorilla, and this difference is apparent in infancy. All G. beringei also have shortened total limb lengths relative to either body mass or vertebral column length, although patterns of variation in individual skeletal elements are more complex, and infants do not display the same patterns as adults. Mountain gorillas have relatively long clavicles, present in infancy, and a relatively long thoracic (but not lumbosacral) vertebral column. DISCUSSION: A variety of environmental factors likely contributed to observed patterns of morphological variation among extant gorillas. We interpret the short hand and foot bones of all G. beringei as genetic adaptations to greater terrestriality in the last common ancestor of G. beringei; variation in other limb lengths to climatic adaptation, both genetic and developmental; and the larger thorax of G. b. beringei to adaptation to reduced oxygen pressure at high altitudes, again as a product of both genetic differences and environmental influences during development.

Phalangeal curvature in a chimpanzee raised like a human: Implications for inferring arboreality in fossil hominins.

Arboreal primates such as chimpanzees exhibit pronounced curvature in their hand and foot phalanges, which is assumed to develop throughout life in response to mechanical loads produced by grasping and hanging from branches. Intriguingly, ancient fossil hominins also exhibit substantial phalangeal curvature, which, too, has been interpreted as a direct result of habitual arboreality during life. Here, we describe the phalangeal curvature of a chimpanzee who was raised during the 1930s in New York City to live much like a human, including by having very few opportunities to engage in arboreal activities. We show that the degree of hand and foot phalangeal curvature in this individual is indistinguishable from that of wild chimpanzees and distinct from humans. Thus, rather than being a direct effect of mechanical loads produced by lifetime arboreal activities, phalangeal curvature appears to be shaped largely by genetic factors. An important implication of this finding is that phalangeal curvature among fossil hominins is evidently best interpreted as a primitive trait inherited from an arboreal ancestral species rather than proof of engagement in arboreal activities during life.

Long bone diaphyseal shape follows different ontogenetic trajectories in captive and wild gorillas.

OBJECTIVES: A number of studies have demonstrated the ontogenetic plasticity of long bone diaphyseal structure in response to mechanical loading. Captivity should affect mechanical loading of the limbs, but whether captive apes grow differently than wild apes has been debated. Here, we compare captive and wild juvenile and adult Gorilla to ascertain whether growth trajectories in cross-sectional diaphyseal shape are similar in the two environments. MATERIALS AND METHODS: A sample of young juvenile (n = 4) and adult (n = 10) captive Gorilla gorilla gorilla specimens, with known life histories, were compared with age-matched wild G.g. gorilla (n = 62) and G. beringei beringei (n = 75) in relative anteroposterior to mediolateral bending strength of the femur, tibia, and humerus. Cross sections were obtained using peripheral quantitative CT. RESULTS: Captive and wild adult G.g. gorilla differed in bending strength ratios for all three bones, but these differences were not present in young juvenile G.g. gorilla. In comparisons across taxa, captive juvenile G.g. gorilla were more similar to wild G.g. gorilla than to G.b. beringei, while captive adult G.g. gorilla were more similar in shape to G.b. beringei in the hind limb. DISCUSSION: Captive and wild G. gorilla follow different ontogenetic trajectories in long bone diaphyseal shape, corresponding to environmental differences and subsequent modified locomotor behaviors. Differences related to phylogeny are most evident early in development.

Phylogenetic and environmental effects on limb bone structure in gorillas.

OBJECTIVES: The effects of phylogeny and locomotor behavior on long bone structural proportions are assessed through comparisons between adult and ontogenetic samples of extant gorillas. MATERIALS AND METHODS: A total of 281 wild-collected individuals were included in the study, divided into four groups that vary taxonomically and ecologically: western lowland gorillas (G. g. gorilla), lowland and highland grauer gorillas (G. b. graueri), and Virunga mountain gorillas (G. b. beringei). Lengths and articular breadths of the major long bones (except the fibula) were measured, and diaphyseal cross-sectional geometric properties determined using computed tomography. Ages of immature specimens (n = 145) were known or estimated from dental development. Differences between groups in hind limb to forelimb proportions were assessed in both adults and during development. RESULTS: Diaphyseal strength proportions among adults vary in parallel with behavioral/ecological differences, and not phylogeny. The more arboreal western lowland and lowland grauer gorillas have relatively stronger forelimbs than the more terrestrial Virunga mountain gorillas, while the behaviorally intermediate highland grauer gorillas have intermediate proportions. Diaphyseal strength proportions are similar in young infants but diverge after 2 years of age in western lowland and mountain gorillas, at the same time that changes in locomotor behavior occur. There are no differences between groups in length or articular proportions among either adults or immature individuals. CONCLUSION: Long bone diaphyseal strength proportions in gorillas are developmentally plastic, reflecting behavior, while length and articular proportions are much more genetically canalized. These findings have implications for interpreting morphological variation among fossil taxa.

Lower limb articular scaling and body mass estimation in Pliocene and Pleistocene hominins.

Previous attempts to estimate body mass in pre-Holocene hominins have relied on prediction equations derived from relatively limited extant samples. Here we derive new equations to predict body mass from femoral head breadth and proximal tibial plateau breadth based on a large and diverse sample of modern humans (avoiding the problems associated with using diaphyseal dimensions and/or cadaveric reference samples). In addition, an adjustment for the relatively small femoral heads of non-Homo taxa is developed based on observed differences in hip to knee joint scaling. Body mass is then estimated for 214 terminal Miocene through Pleistocene hominin specimens. Mean body masses for non-Homo taxa range between 39 and 49 kg (39-45 kg if sex-specific means are averaged), with no consistent temporal trend (6-1.85 Ma). Mean body mass increases in early Homo (2.04-1.77 Ma) to 55-59 kg, and then again dramatically in Homo erectus and later archaic middle Pleistocene Homo, to about 70 kg. The same average body mass is maintained in late Pleistocene archaic Homo and early anatomically modern humans through the early/middle Upper Paleolithic (0.024 Ma), only declining in the late Upper Paleolithic, with regional variation. Sexual dimorphism in body mass is greatest in Australopithecus afarensis (log[male/female] = 1.54), declines in Australopithecus africanus and Paranthropus robustus (log ratio 1.36), and then again in early Homo and middle and late Pleistocene archaic Homo (log ratio 1.20-1.27), although it remains somewhat elevated above that of living and middle/late Pleistocene anatomically modern humans (log ratio about 1.15).

Body mass estimation in hominoids: Age and locomotor effects.

While there are a number of methods available for estimation of body mass in adult nonhuman primates, very few are available for juveniles, despite the potential utility of such estimations in both analyses of fossils and in museum collection based research. Furthermore, because of possible scaling differences, adult based body mass estimation equations may not be appropriate for non-adults. In this study, we present new body mass estimation equations for both adult and immature nonhuman hominoids based on joint and metaphyseal dimensions. Articular breadths of the proximal and distal femur, distal humerus and tibial plateau, and metaphyseal breadths of the distal femur and humerus were collected on a reference sample of 159 wild Pan, Gorilla, Pongo, Hylobates, and Symphalangus specimens of known body mass from museum and research collections. Scaling of dimensions with body weight was assessed in both the adult and the ontogenetic sample at several taxonomic levels using reduced major axis regression, followed by regression of each dimension against body mass to generate body mass estimation equations. Joint dimensions were found to be good predictors of body mass in both adult and immature hominoids, with percent prediction errors of 10-20%. However, subtle scaling differences between taxa impacted body mass estimation, suggesting that phylogeny and locomotor effects should be considered when selecting reference samples. Unlike patterns of joint growth in humans, there was little conclusive evidence for consistently larger joints relative to body mass in the non-adult sample. Metaphyseal breadths were strong predictors of body mass and, with some exceptions, gave more precise body mass estimates for non-adults than epiphyseal breadths.

Articular scaling and body mass estimation in platyrrhines and catarrhines: Modern variation and application to fossil anthropoids.

Body mass is an important component of any paleobiological reconstruction. Reliable skeletal dimensions for making estimates are desirable but extant primate reference samples with known body masses are rare. We estimated body mass in a sample of extinct platyrrhines and Fayum anthropoids based on four measurements of the articular surfaces of the humerus and femur. Estimates were based on a large extant reference sample of wild-collected individuals with associated body masses, including previously published and new data from extant platyrrhines, cercopithecoids, and hominoids. In general, scaling of joint dimensions is positively allometric relative to expectations of geometric isometry, but negatively allometric relative to expectations of maintaining equivalent joint surface areas. Body mass prediction equations based on articular breadths are reasonably precise, with %SEEs of 17-25%. The breadth of the distal femoral articulation yields the most reliable estimates of body mass because it scales similarly in all major anthropoid taxa. Other joints scale differently in different taxa; therefore, locomotor style and phylogenetic affinity must be considered when calculating body mass estimates from the proximal femur, proximal humerus, and distal humerus. The body mass prediction equations were applied to 36 Old World and New World fossil anthropoid specimens representing 11 taxa, plus two Haitian specimens of uncertain taxonomic affinity. Among the extinct platyrrhines studied, only Cebupithecia is similar to large, extant platyrrhines in having large humeral (especially distal) joints. Our body mass estimates differ from each other and from published estimates based on teeth in ways that reflect known differences in relative sizes of the joints and teeth. We prefer body mass estimators that are biomechanically linked to weight-bearing, and especially those that are relatively insensitive to differences in locomotor style and phylogenetic history. Whenever possible, extant reference samples should be chosen to match target fossils in joint proportionality.

Limb Bone Structural Proportions and Locomotor Behavior in A.L. 288-1 ("Lucy").

While there is broad agreement that early hominins practiced some form of terrestrial bipedality, there is also evidence that arboreal behavior remained a part of the locomotor repertoire in some taxa, and that bipedal locomotion may not have been identical to that of modern humans. It has been difficult to evaluate such evidence, however, because of the possibility that early hominins retained primitive traits (such as relatively long upper limbs) of little contemporaneous adaptive significance. Here we examine bone structural properties of the femur and humerus in the Australopithecus afarensis A.L. 288-1 ("Lucy", 3.2 Myr) that are known to be developmentally plastic, and compare them with other early hominins, modern humans, and modern chimpanzees. Cross-sectional images were obtained from micro-CT scans of the original specimens and used to derive section properties of the diaphyses, as well as superior and inferior cortical thicknesses of the femoral neck. A.L. 288-1 shows femoral/humeral diaphyseal strength proportions that are intermediate between those of modern humans and chimpanzees, indicating more mechanical loading of the forelimb than in modern humans, and by implication, a significant arboreal locomotor component. Several features of the proximal femur in A.L. 288-1 and other australopiths, including relative femoral head size, distribution of cortical bone in the femoral neck, and cross-sectional shape of the proximal shaft, support the inference of a bipedal gait pattern that differed slightly from that of modern humans, involving more lateral deviation of the body center of mass over the support limb, which would have entailed increased cost of terrestrial locomotion. There is also evidence consistent with increased muscular strength among australopiths in both the forelimb and hind limb, possibly reflecting metabolic trade-offs between muscle and brain development during hominin evolution. Together these findings imply significant differences in both locomotor behavior and ecology between australopiths and later Homo.

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.

How much more would KNM-WT 15000 have grown?

Because of its completeness, the juvenile Homo ergaster/erectus KNM-WT 15000 has played an important role in studies of the evolution of body form in Homo. Early attempts to estimate his adult body size used modern human growth models. However, more recent evidence, particularly from the dentition, suggests that he may have had a more chimpanzee-like growth trajectory. Here we re-estimate his adult stature and body mass using ontogenetic data derived from four African ape taxa: Pan troglodytes troglodytes, Pan troglodytes schweinfurthii, Pan paniscus, and Gorilla gorilla gorilla. The average percentage change in femoral and tibial lengths and femoral head breadth between individuals at the same stage of dental development as KNM-WT 15000 - eruption of M2s but not M3s - and adult individuals with fully fused long bone epiphyses, was determined. Results were then applied to KNM-WT 15000, and his adult size estimated from skeletal dimensions using modern human prediction formulae. Using this approach, adult stature best estimates of 176-180 cm and body mass best estimates of 80-83 kg were obtained. These estimates are close to those estimated directly from longitudinal changes in body length and body mass between 8 and 12 years of age in chimpanzees, the suggested chronological equivalent to KNM-WT 15000's remaining growth period. Thus, even using an African ape growth model, it is likely that KNM-WT 15000 would have attained close to 180 cm in stature (without a slight reduction for his lower cranial height) and 80 kg in body mass as an adult. Other evidence from the East African Early Pleistocene indicates that KNM-WT 15000 was not unusually large-bodied for his time period.

Ontogenetic changes in limb bone structural proportions in mountain gorillas (Gorilla beringei beringei).

Behavioral studies indicate that adult mountain gorillas (Gorilla beringei) are the most terrestrial of all nonhuman hominoids, but that infant mountain gorillas are much more arboreal. Here we examine ontogenetic changes in diaphyseal strength and length of the femur, tibia, humerus, radius, and ulna in 30 Virunga mountain gorillas, including 18 immature specimens and 12 adults. Comparisons are also made with 14 adult western lowland gorillas (Gorilla gorilla gorilla), which are known to be more arboreal than adult mountain gorillas. Infant mountain gorillas have significantly stronger forelimbs relative to hind limbs than older juveniles and adults, but are nonsignificantly different from western lowland gorilla adults. The change in inter-limb strength proportions is abrupt at about two years of age, corresponding to the documented transition to committed terrestrial quadrupedalism in mountain gorillas. The one exception is the ulna, which shows a gradual increase in strength relative to the radius and other long bones during development, possibly corresponding to the gradual adoption of stereotypical fully pronated knuckle-walking in older juvenile gorillas. Inter-limb bone length proportions show a contrasting developmental pattern, with hind limb/forelimb length declining rapidly from birth to five months of age, and then showing no consistent change through adulthood. The very early change in length proportions, prior to significant independent locomotion, may be related to the need for relatively long forelimbs for climbing in a large-bodied hominoid. Virunga mountain gorilla older juveniles and adults have equal or longer forelimb relative to hind limb bones than western lowland adults. These findings indicate that both ontogenetically and among closely related species of Gorilla, long bone strength proportions better reflect actual locomotor behavior than bone length proportions.