Facial asymmetry tracks genetic diversity among Gorilla subspecies.

Mountain gorillas are particularly inbred compared to other gorillas and even the most inbred human populations. As mountain gorilla skeletal material accumulated during the 1970s, researchers noted their pronounced facial asymmetry and hypothesized that it reflects a population-wide chewing side preference. However, asymmetry has also been linked to environmental and genetic stress in experimental models. Here, we examine facial asymmetry in 114 crania from three Gorilla subspecies using 3D geometric morphometrics. We measure fluctuating asymmetry (FA), defined as random deviations from perfect symmetry, and population-specific patterns of directional asymmetry (DA). Mountain gorillas, with a current population size of about 1000 individuals, have the highest degree of facial FA (explaining 17% of total facial shape variation), followed by Grauer gorillas (9%) and western lowland gorillas (6%), despite the latter experiencing the greatest ecological and dietary variability. DA, while significant in all three taxa, explains relatively less shape variation than FA does. Facial asymmetry correlates neither with tooth wear asymmetry nor increases with age in a mountain gorilla subsample, undermining the hypothesis that facial asymmetry is driven by chewing side preference. An examination of temporal trends shows that stress-induced developmental instability has increased over the last 100 years in these endangered apes.

In vivo deciduous dental eruption in LuiKotale bonobos and Gombe chimpanzees.

OBJECTIVES: Existing data on bonobo and chimpanzee dental eruption timing are derived predominantly from captive individuals or deceased wild individuals. However, recent advances in noninvasive photographic monitoring of living, wild apes have enabled researchers to characterize dental eruption in relatively healthy individuals under naturalistic conditions. At present, such data are available for only one population of wild chimpanzees. We report data for an additional population of wild chimpanzees and the first dental eruption data for wild bonobos. MATERIALS AND METHODS: We collected photographs and video footage of teeth from the open mouths of wild bonobos and East African chimpanzees of known age from LuiKotale, Democratic Republic of the Congo, and Gombe National Park, Tanzania, respectively. We scored the presence and absence of deciduous teeth from photographs and video footage to characterize deciduous dental eruption timing in these two populations. RESULTS: Deciduous dental eruption ages in our sample fall within the range of variation previously documented for captive chimpanzees, but eruption ages are later in wild than in captive contexts. We found substantial variation in deciduous canine eruption timing, particularly among bonobos. One bonobo had a deciduous canine present by 227 days old while another did not have a deciduous canine present at 477 days old. DISCUSSION: Our data indicate that deciduous teeth erupt later in wild individuals than in captive individuals. We also found that deciduous dental eruption timing varies considerably between individuals within our study populations, a pattern that is consistent with previous studies. Future studies should consider sources of variation in deciduous canine eruption timing and relationships with other aspects of life history as additional data become available.

Pelvic shape variation among gorilla subspecies: Phylogenetic and ecological signals.

Gorillas occupy habitats that range in elevation from 0 to 3850 m. Populations at higher elevations tend to be less arboreal than lowland populations. Variation in habitat-specific behaviors among closely related populations makes gorillas a unique model to study the relationship between locomotion and morphology. The pelvis reflects differences in locomotion in other primates, and thus may also reflect locomotor differences among gorillas. We tested the hypothesis that pelvic morphology exhibits clinal variation across elevation within Gorilla. Using 3D geometric morphometrics and principal components analysis (PCA), we characterized pelvic shape in three gorilla subspecies representing 14 localities across gorillas' full elevation range: western lowland gorillas (Gorilla gorilla gorilla), mountain gorillas (Gorilla beringei beringei), and Grauer's gorillas (Gorilla beringei graueri). We found that the first principal component (PC1) usually reflects differences between western and eastern gorillas in the lateral margin of the ilium and, in males, the obturator foramen. When sexes are considered together, the second principal component (PC2) indicates some separation between G. b. beringei and G. b. graueri, albeit with considerable overlap, corresponding to the shape of the iliac crest. When sexes were analyzed separately, there was no distinction. Phylogenetic generalized least squares regression was used to evaluate the relationship between elevation and pelvic shape under varying phylogenetic assumptions. Models were compared to assess how phylogenetic adjustment affects model fit. Neither of the first two PCs nor overall shape yielded a significant relationship with elevation in any of the pooled-sex and individual-sex samples. This suggests that covariation between pelvic morphology and elevation is sex-specific and dependent on phylogenetic assumptions. Our results find complex interactions between sex, phylogeny, elevation, and pelvic morphology, suggesting that there is not one ecomorphological pattern that characterizes all gorillas.

Faster growth corresponds with shallower linear hypoplastic defects in great ape canines.

Deeper or more 'severe' linear enamel hypoplasia (LEH) defects are hypothesized to reflect more severe stress during development, but it is not yet clear how depth is influenced by intrinsic enamel growth patterns. Recent work documented inter- and intraspecific differences in LEH defect depth in extant great apes, with mountain gorillas having shallower defects than other taxa, and females having deeper defects than males. Here, we assess the correspondence of inter- and intraspecific defect depth and intrinsic aspects of enamel growth: enamel extension rates, outer enamel striae of Retzius angles, and linear enamel thickness. Thin sections of great ape canines (n = 40) from Gorilla beringei beringei, Gorilla gorilla gorilla, Pan troglodytes, and Pongo spp. were analyzed. Enamel extension rates were calculated within deciles of enamel-dentine junction length. Linear enamel thickness and the angle of intersection between striae of Retzius and the outer enamel surface were measured in the imbricational enamel. Mountain gorillas have faster enamel extension rates and shallower striae angles than the other taxa examined. Mountain gorillas have thinner imbricational enamel than western lowland gorillas and orangutans, but not chimpanzees. In the combined-taxon sample, females exhibit larger striae angles and thicker imbricational enamel than males. Enamel extension rates are highly negatively correlated with striae angles and LEH defect depth. Enamel growth variation corresponds with documented inter- and intraspecific differences in LEH defect depth in great ape canines. Mountain gorillas have shallower striae angles and faster extension rates than other taxa, which might explain their shallow LEH defect morphology and the underestimation of their LEH prevalence in previous studies. These results suggest that stressors of similar magnitude and timing might produce defects of different depths in one species or sex vs. another, which has implications for interpretations of stress histories in hominins with variable enamel growth patterns.

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.

Incisor tooth wear and age determination in mountain gorillas from Volcanoes National Park, Rwanda.

OBJECTIVES: Ecological factors, but also tooth-to-tooth contact over time, have a dramatic effect on tooth wear in primates. The aim of this study is to test whether incisor tooth wear changes predictably with age and can thus be used as an age estimation method in a wild population of mountain gorillas (Gorilla beringei beringei) from Volcanoes National Park, Rwanda. MATERIALS AND METHODS: In mountain gorillas of confidently known chronological age (N = 24), we measured the crown height of all permanent maxillary and mandibular incisors (I1 , I1 , I2 , I2 ) as a proxy for incisal macrowear. Linear and quadratic regressions for each incisor were used to test whether age can be predicted by crown height. Using these models, we then predicted age at death of two individual mountain gorillas of probable identifications, based on their incisor crown height. RESULTS: Age decreased significantly with incisor height for all teeth, but the upper first incisors (I1 ) provided the best results, with the lowest Akaike's Information Criterion corrected for small sample size (AICc) and lowest Standard Error of the Estimate (SEE). When the best age equations for each sex were applied to gorillas with probable identifications, the predicted ages differed 1.58 and 3.33 years from the probable ages of these individuals. CONCLUSIONS: Our findings corroborate that incisor crown height, a proxy for incisal wear, varies predictably with age. This relationship can be used to estimate age at death of unknown gorillas in the skeletal collection, and in some cases, to corroborate the identity of individual gorillas recovered from the forest postmortem at an advanced state of decomposition. Such identifications help fill gaps in the demographic database and support research that requires individual-level data.

Unexpected terrestrial hand posture diversity in wild mountain gorillas.

OBJECTIVES: Gorillas, along with chimpanzees and bonobos, are ubiquitously described as 'knuckle-walkers.' Consequently, knuckle-walking (KW) has been featured pre-eminently in hypotheses of the pre-bipedal locomotor behavior of hominins and in the evolution of locomotor behavior in apes. However, anecdotal and behavioral accounts suggest that mountain gorillas may utilize a more complex repertoire of hand postures, which could alter current interpretations of African ape locomotion and its role in the emergence of human bipedalism. Here we documented hand postures during terrestrial locomotion in wild mountain gorillas to investigate the frequency with which KW and other hand postures are utilized in the wild. MATERIALS AND METHODS: Multiple high-speed cameras were used to record bouts of terrestrial locomotion of 77 habituated mountain gorillas at Bwindi Impenetrable National Park (Uganda) and Volcanoes National Park (Rwanda). RESULTS: We captured high-speed video of hand contacts in 8% of the world's population of mountain gorillas. Our results reveal that nearly 40% of these gorillas used "non-KW" hand postures, and these hand postures constituted 15% of all hand contacts. Some of these "non-KW" hand postures have never been documented in gorillas, yet match hand postures previously identified in orangutans. DISCUSSION: These results highlight a previously unrecognized level of hand postural diversity in gorillas, and perhaps great apes generally. Although present at lower frequencies than KW, we suggest that the possession of multiple, versatile hand postures present in wild mountain gorillas may represent a shared feature of the African ape and human clade (or even great ape clade) rather than KW per se.

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.

Quantifying linear enamel hypoplasia in Virunga Mountain gorillas and other great apes.

OBJECTIVE: Linear enamel hypoplasia (LEH) is a condition marked by localized reductions in enamel thickness, resulting from growth disruptions during dental development. We use quantitative criteria to characterize the depth of LEH defects and "normal" perikymata in great apes. We test the hypothesis that mountain gorillas have shallow defects compared to other taxa, which may have led to their underestimation in previous studies. MATERIALS AND METHODS: Previous attempts to characterize LEH morphology quantitatively have been limited in sample size and scope. We generated digital elevation models using optical profilometry (Sensofar PLu Neox) and extracted 2D coordinates using ImageJ to quantify depths in canines from three great ape genera (N = 75 perikymata; 255 defects). RESULTS: All defect depths fall outside the distribution of perikymata depths. Mountain gorilla defects are significantly shallower than those of other great ape taxa examined, including western lowland gorillas. Females have significantly deeper defects than males in all taxa. The deepest defect belongs to a wild-captured zoo gorilla. Virunga mountain gorilla specimens collected by Dian Fossey exhibit deeper defects than those collected recently. DISCUSSION: Shallow defect morphology in mountain gorillas may have led to an underestimation of LEH prevalence in past studies. Defect depth is used as a proxy for insult severity, but depth might be influenced by inter- and intra-specific variation in enamel growth. Future studies should test whether severe insults are associated with deeper defects, as might be the case with Haloko, a wild-captured gorilla. Ongoing histologic studies incorporating associated behavioral records will test possible factors that underlie differences in defect morphology.

Body growth and life history in wild mountain gorillas (Gorilla beringei beringei) from Volcanoes National Park, Rwanda.

OBJECTIVES: Great apes show considerable diversity in socioecology and life history, but knowledge of their physical growth in natural settings is scarce. We characterized linear body size growth in wild mountain gorillas from Volcanoes National Park, Rwanda, a population distinguished by its extreme folivory and accelerated life histories. METHODS: In 131 individuals (0.09-35.26 years), we used non-invasive parallel laser photogrammetry to measure body length, back width, arm length and two head dimensions. Nonparametric LOESS regression was used to characterize cross-sectional distance and velocity growth curves for males and females, and consider links with key life history milestones. RESULTS: Sex differences became evident between 8.5 and 10.0 years of age. Thereafter, female growth velocities declined, while males showed increased growth velocities until 10.0-14.5 years across dimensions. Body dimensions varied in growth; females and males reached 98% of maximum body length at 11.7 and 13.1 years, respectively. Females attained 95.3% of maximum body length by mean age at first birth. Neonates were 31% of maternal size, and doubled in size by mean weaning age. Males reached maximum body and arm length and back width before emigration, but experienced continued growth in head dimensions. CONCLUSIONS: While comparable data are scarce, our findings provide preliminary support for the prediction that mountain gorillas reach maximum body size at earlier ages compared to more frugivorous western gorillas. Data from other wild populations are needed to better understand comparative great ape development, and investigate links between trajectories of physical, behavioral, and reproductive maturation.

A radiographic study of permanent molar development in wild Virunga mountain gorillas of known chronological age from Rwanda.

OBJECTIVES: While dental development is important to life history investigations, data from wild known-aged great apes are scarce. We report on the first radiographic examination of dental development in wild Virunga mountain gorillas, using known-age skeletal samples recovered in Rwanda. MATERIALS AND METHODS: In 43 individuals (0.0-14.94 years), we collected radiographs of mandibular molars, and where possible, cone beam CT scans. Molar crown and root calcification status was assessed using two established staging systems, and age prediction equations generated using polynomial regression. Results were compared to available data from known-age captive and wild chimpanzees. RESULTS: Mountain gorillas generally fell within reported captive chimpanzee distributions or exceeded them, exhibiting older ages at equivalent radiographic stages of development. Differences reflect delayed initiation and/or an extended duration of second molar crown development, and extended first and second molar root development, in mountain gorillas compared to captive chimpanzees. However, differences in the duration of molar root development were less evident compared to wild chimpanzees. DISCUSSION: Despite sample limitations, our findings extend the known range of variation in radiographic estimates of molar formation timing in great apes, and provide a new age prediction technique based on wild specimens. However, mountain gorillas do not appear accelerated in radiographic assessment of molar formation compared to chimpanzees, as they are for other life history traits. Future studies should aim to resolve the influence of species differences, wild versus captive environments, and/or sampling phenomena on patterns observed here, and more generally, how they relate to variation in tooth size, eruption timing, and developmental life history.

Toughness of the Virunga mountain gorilla (Gorilla beringei beringei) diet across an altitudinal gradient.

The robust masticatory system of mountain gorillas is thought to have evolved for the comminution of tough vegetation, yet, compared to other primates, the toughness of the mountain gorilla diet is unremarkable. This may be a result of low plant toughness in the mountain gorilla environment or of mountain gorillas feeding selectively on low-toughness foods. The goal of this paper is to determine how the toughness of the mountain gorilla diet varies across their habitat, which spans a large altitudinal range, and whether there is a relationship between toughness and food selection by mountain gorillas. We collected data on the following variables to determine whether, and if so how, they change with altitude: leaf toughness of two plant species consumed by mountain gorillas, at every 100 m increase in altitude (2,600-3,700 m); toughness of consumed foods comprising over 85% of the gorilla diet across five vegetation zones; and toughness of unconsumed/infrequently consumed plant parts of those foods. Although leaf toughness increased with altitude, the toughness of the gorilla diet remained similar. There was a negative relationship between toughness and consumption frequency, and toughness was a better predictor of consumption frequency than plant frequency, biomass, and density. Consumed plant parts were less tough than unconsumed/infrequently consumed parts and toughness of the latter increased with altitude. Although it is unclear whether gorillas select food based on toughness or use toughness as a sensory cue to impart other plant properties (e.g., macronutrients, chemicals), our results that gorillas maintain a consistent low-toughness dietary profile across altitude, despite toughness increasing with altitude, suggest that the robust gorilla masticatory apparatus evolved for repetitive mastication of foods that are not high in toughness.

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.

Age-related changes in molar topography and shearing crest length in a wild population of mountain Gorillas from Volcanoes National Park, Rwanda.

OBJECTIVES: Great ape teeth must remain functional over long lifespans. The molars of the most folivorous apes, the mountain gorillas, must maintain shearing function for 40+ years while the animals consume large quantities of mechanically challenging foods. While other folivorous primates experience dental senescence, which compromises their occlusal surfaces and affects their reproductive success as they age, it is unknown whether dental senescence also occurs in mountain gorillas. In this article, we quantified and evaluated how mountain gorilla molars change throughout their long lifespans. MATERIALS AND METHODS: We collected high-resolution replicas of M(1)s (n = 15), M(2)s (n = 13), and M(3)s (n = 11) from a cross-sectional sample of wild mountain gorilla skeletons from the Virunga Volcanoes, ranging in age from 4 to 43 years. We employed dental topographic analyses to track how aspects of occlusal slope, angularity, relief index, and orientation patch count rotated change with age. In addition, we measured the relative length of shearing crests in two- and three-dimensions. RESULTS: Occlusal topography was found to decrease, while 2D relative shearing crest length increased, and 3D relative crest lengths were maintained with age. DISCUSSION: Our findings indicate that shearing function is maintained throughout the long lifetimes of mountain gorillas. Unlike the dental senescence experienced by other folivorous primates, mountain gorillas do not appear to possess senesced molars despite their long lifetimes, mechanically challenging diets, and decreases in occlusal topography with age.

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.

Tooth wear and feeding ecology in mountain gorillas from Volcanoes National Park, Rwanda.

OBJECTIVES: Ecological factors have a dramatic effect on tooth wear in primates, although it remains unclear how individual age contributes to functional crown morphology. The aim of this study is to determine how age and individual diet are related to tooth wear in wild mountain gorillas (Gorilla beringei beringei) from Volcanoes National Park, Rwanda. MATERIAL AND METHODS: We calculated the percent of dentine exposure (PDE) for all permanent molars (M1-M3) of known-age mountain gorillas (N = 23), to test whether PDE varied with age using regression analysis. For each molar position, we also performed stepwise multiple linear regression to test the effects of age and percentage of time spent feeding on different food categories on PDE, for individuals subject to long-term observational studies by the Dian Fossey Gorilla Fund International's Karisoke Research Center. RESULTS: PDE increased significantly with age for both sexes in all molars. Moreover, a significant effect of gritty plant root consumption on PDE was found among individuals. Our results support prior reports indicating reduced tooth wear in mountain gorillas compared to western gorillas, and compared to other known-aged samples of primate taxa from forest and savanna habitats. DISCUSSION: Our findings corroborate that mountain gorillas present very low molar wear, and support the hypothesis that age and the consumption of particular food types, namely roots, are significant determinants of tooth wear variation in mountain gorillas. Future research should characterize the mineral composition of the soil in the Virunga habitat, to test the hypothesis that the physical and abrasive properties of gritty foods such as roots influence intra- and interspecific patterns of tooth wear.

The evolutionary origin and population history of the grauer gorilla.

Gorillas living in western central Africa (Gorilla gorilla) are morphologically and genetically distinguishable from those living in eastern central Africa (Gorilla beringei). Genomic analyses show eastern gorillas experienced a significant reduction in population size during the Pleistocene subsequent to geographical isolation from their western counterparts. However, how these results relate more specifically to the recent biogeographical and evolutionary history of eastern gorillas remains poorly understood. Here we show that two rare morphological traits are present in the hands and feet of both eastern gorilla subspecies at strikingly high frequencies (>60% in G. b. graueri; ∼28% in G. b. beringei) in comparison with western gorillas (<1%). The intrageneric distribution of these rare traits suggests that they became common among eastern gorillas after diverging from their western relatives during the early to middle Pleistocene. The extremely high frequencies observed among grauer gorillas-which currently occupy a geographic range more than ten times the size of that of mountain gorillas-imply that grauers originated relatively recently from a small founding population of eastern gorillas. Current paleoenvironmental, geological, and biogeographical evidence supports the hypothesis that a small group of eastern gorillas likely dispersed westward from the Virungas into present-day grauer range in the highlands just north of Lake Kivu, either immediately before or directly after the Younger Dryas interval. We propose that as the lowland forests of central Africa expanded rapidly during the early Holocene, they became connected with the expanding highland forests along the Albertine Rift and enabled the descendants of this small group to widely disperse. The descendant populations significantly expanded their geographic range and population numbers relative to the gorillas of the Virunga Mountains and the Bwindi-Impenetrable Forest, ultimately resulting in the grauer gorilla subspecies recognized today. This founder-effect hypothesis offers some optimism for modern conservation efforts to save critically endangered eastern gorillas from extinction.

Validation of two independent photogrammetric techniques for determining body measurements of gorillas.

The ability to accurately measure morphological characteristics of wild primates in the field is challenging, yet critical for understanding fundamental aspects of their biology and behavior. Recent studies have shown that digital photogrammetry can be used to non-invasively measure morphological traits of wild primates, as it allows for the determination of geometric properties of objects remotely from photographic images. We report here on a rare opportunity to test this methodology by comparing measurements obtained directly from living great apes to those obtained from photographs. We test the accuracy and precision of two independent photogrammetric techniques, employing the use of parallel lasers and a distance meter, respectively, for obtaining measurements of static objects and captive western lowland gorillas (Gorilla gorilla gorilla) (n = 4) at Zoo Atlanta. For static objects, the mean percent error between corresponding measurements collected by the same observer directly versus using photogrammetry was 0.49-0.74% for the parallel laser method and 0.62-0.76% for the distance meter method. For gorillas, mean percent error between corresponding direct and remote measurements was 2.72-5.20% for the parallel laser method and 2.20-7.51% for the distance meter method. Correlations between direct measurements and corresponding parallel laser and distance meter measurements of gorillas were highly significant with R2 values and slopes approaching 1.0 (parallel lasers: R2 = 0.9989, P < 0.0001; distance-meter: R2 = 0.9990, P < 0.0001). Further, variation between measurements of the same targets collected repeatedly by the same observer, and between different observers, was uniformly low across methods (CV, range = 0.003-0.013). While errors are slightly higher for the distance meter technique, both methods show great promise for addressing a wide range of questions requiring the non-invasive collection of morphological data from wild primates. Am. J. Primatol. 78:418-431, 2016. © 2015 Wiley Periodicals, Inc.

Comparative analysis of Meissner's corpuscles in the fingertips of primates.

Meissner's corpuscles (MCs) are tactile mechanoreceptors found in the glabrous skin of primates, including fingertips. These receptors are characterized by sensitivity to light touch, and therefore might be associated with the evolution of manipulative abilities of the hands in primates. We examined MCs in different primate species, including common marmoset (Callithrix jacchus, n = 5), baboon (Papio anubis, n = 2), rhesus macaque (Macaca mulatta, n = 3), chimpanzee (Pan troglodytes, n = 3), bonobo (Pan paniscus, n = 1) and human (Homo sapiens, n = 8). Fingertips of the first, second and fourth digits were collected from both hands of specimens, dissected and histologically stained using hematoxylin and eosin. The density (MCs per 1 mm(2) ) and the size (cross-sectional diameter of MCs) were quantified. Overall, there were no differences in the densities of MCs or their size among the digits or between the hands for any species examined. However, MCs varied across species. We found a trend for higher densities of MCs in macaques and humans compared with chimpanzees and bonobos; moreover, apes had larger MCs than monkeys. We further examined whether the density or size of MCs varied as a function of body mass, measures of dexterity and dietary frugivory. Among these variables, only body size accounted for a significant amount of variation in the size of MCs.

Locomotor activity influences muscle architecture and bone growth but not muscle attachment site morphology.

The ability to make behavioural inferences from skeletal remains is critical to understanding the lifestyles and activities of past human populations and extinct animals. Muscle attachment site (enthesis) morphology has long been assumed to reflect muscle strength and activity during life, but little experimental evidence exists to directly link activity patterns with muscle development and the morphology of their attachments to the skeleton. We used a mouse model to experimentally test how the level and type of activity influences forelimb muscle architecture of spinodeltoideus, acromiodeltoideus, and superficial pectoralis, bone growth rate and gross morphology of their insertion sites. Over an 11-week period, we collected data on activity levels in one control group and two experimental activity groups (running, climbing) of female wild-type mice. Our results show that both activity type and level increased bone growth rates influenced muscle architecture, including differences in potential muscular excursion (fibre length) and potential force production (physiological cross-sectional area). However, despite significant influences on muscle architecture and bone development, activity had no observable effect on enthesis morphology. These results suggest that the gross morphology of entheses is less reliable than internal bone structure for making inferences about an individual's past behaviour.