Ontogenetic variation in the mandibular ramus of great apes and humans

Considerable variation exists in mandibular ramus form among primates, particularly great apes and humans. Recent analyses of adult ramal morphology have suggested that features on the ramus, especially the coronoid process and sigmoid notch, can be treated as phylogenetic characters that can be used to reconstruct relationships among great ape and fossil hominin taxa. Others have contended that ramal morphology is more influenced by function than phylogeny. In addition, it remains unclear how ontogeny of the ramus contributes to adult variation in great apes and humans. Specifically, it is unclear whether differences among adults appear early and are maintained throughout ontogeny, or if these differences appear, or are enhanced, during later development. To address these questions, the present study examined a broad ontogenetic sample of great apes and humans using two‐dimensional geometric morphometric analysis. Variation within and among species was summarized using principal component and thin plate spline analyses, and Procrustes distances and discriminant function analyses were used to statistically compare species and age classes. Results suggest that morphological differences among species in ramal morphology appear early in ontogeny and persist into adulthood. Morphological differences among adults are particularly pronounced in the height and angulation of the coronoid process, the depth and anteroposterior length of the sigmoid notch, and the inclination of the ramus. In all taxa, the ascending ramus of the youngest specimens is more posteriorly inclined in relation to the occlusal plane, shifting to become more upright in adults. These results suggest that, although there are likely functional influences over the form of the coronoid process and ramus, the morphology of this region can be profitably used to differentiate among great apes, modern humans, and fossil hominid taxa. J. Morphol. 275:661–677, 2014. © 2013 Wiley Periodicals, Inc.     

Locomotor variation and bending regimes of capuchin limb bones

Primates are very versatile in their modes of progression, yet laboratory studies typically capture only a small segment of this variation. In vivo bone strain studies in particular have been commonly constrained to linear locomotion on flat substrates, conveying the potentially biased impression of stereotypic long bone loading patterns. We here present substrate reaction forces (SRF) and limb postures for capuchin monkeys moving on a flat substrate (“terrestrial”), on an elevated pole (“arboreal”), and performing turns. The angle between the SRF vector and longitudinal axes of the forearm or leg is taken as a proxy for the bending moment experienced by these limb segments. In both frontal and sagittal planes, SRF vectors and distal limb segments are not aligned, but form discrepant angles; that is, forces act on lever arms and exert bending moments. The positions of the SRF vectors suggest bending around oblique axes of these limb segments. Overall, the leg is exposed to greater moments than the forearm. Simulated arboreal locomotion and turns introduce variation in the discrepancy angles, thus confirming that expanding the range of locomotor behaviors studied will reveal variation in long bone loading patterns that is likely characteristic of natural locomotor repertoires. “Arboreal” locomotion, even on a linear noncompliant branch, is characterized by greater variability of force directions and discrepancy angles than “terrestrial” locomotion (significant for the forearm only), partially confirming the notion that life in trees is associated with greater variation in long bone loading. Directional changes broaden the range of external bending moments even further. Am J Phys Anthropol, 2009. © 2009 Wiley‐Liss, Inc.     

Relationship of strain magnitude to morphological variation in the primate skull

In a comparative study of variation in primate skulls, Wood and Lieberman ([ 2001 ] Am. J. Phys. Anthropol. 116:13–25) proposed that a predictable relationship exists between in vivo bone‐strain magnitudes and the extent of morphological variation in skeletal structures. They hypothesized that regions subject to high strains are prone to enhanced levels of variation. Three questions are posed with respect to the plausibility of this hypothesis. First, does the proposed relationship hold at different levels of analysis (e.g., for more restricted anatomical regions in which large strain gradients are present)? Second, is the biomechanical rationale for the hypothesis sound, given the current understanding of bone biology? Third, is the hypothesis obviated by consideration of the functional matrix concept of skull development, in which osseous growth is posited to be governed by surrounding soft tissues (e.g., muscle and tendon) and developing spaces (e.g., the nasal capsule)? The different perspectives explored by these questions suggest that the validity of the hypothesis, despite having a defensible theoretical rationale, is likely to be context‐specific. A direct role for strain magnitude in conditioning morphological variation is difficult to demonstrate either comparatively or theoretically, and it is unlikely that a single strain threshold or interval can be directly associated with elevated variation in the skeleton. The conceptual framework of the functional matrix (which allows for independent growth among different regions of the skull) conceivably contravenes the premise of a uniform relationship of strain magnitude to morphological variability. Am J Phys Anthropol, 2003. © 2003 Wiley‐Liss, Inc.     

Estimating the length of incomplete long bones: forensic standards from Guatemala

We report on new standards for estimating long bone length from incomplete bones for use in forensic and archaeological contexts in Central America. The measurements we use closely follow those defined by Steele ([1970] Personal Identification in Mass Disasters; Washington, DC: Smithsonian Institution), but we add several new landmarks. We measured the femur, humerus, tibia, and fibula of 100 Maya skeletons (68 males, 32 females) recovered from forensic exhumations. We derived the equations by regressing bone segment length on bone length, and solved for bone length to maximize the utility of the equations for taller populations. We generated equations for all segments that were significantly correlated with bone length for males, for females, and for both sexes combined, but accepted only regressions with r(2) > 0.85 as reliable. Landmarks defined by muscle attachment sites were more variable in location than landmarks on articular architecture; thus we retained few equations that use these landmarks. We tested the male and combined sex equations on 36 males of unknown ethnicity exhumed from a military base in Guatemala, and found that the equations performed satisfactorily. We also evaluated the performance of equations by Steele ([1970] Personal Identification in Mass Disasters; Washington, DC: Smithsonian Institution) and Jacobs ([1992] Am J Phys Anthropol 89:333-345) on the Maya bones, and conclude that significant population variation in long bone proportions hinders their application in Central America.     

Ecological associations of autopodial osteology in Neotropical geckos

Coevolution of form and function inspires investigation of associations between morphological variation and the exploitation of specific ecological settings. Such relationships, based mostly on traits of external morphology, have been extensively described for vertebrates, and especially so for squamates. External features are, however, composed by both soft tissues and bones, and these likely play different biomechanical roles during locomotion, such as in the autopodia. Therefore, ecological trends identified on the basis of external morphological measurements may not be directly correlated with equivalent variation in osteology. Here, we investigate how refined parameters of autopodial osteology relate to ecology, by contrasting climbing and nonclimbing geckos. Our first step consisted of inferring how external and osteological morphometric traits coevolved in the group. Our results corroborate the hypothesis of coevolution between external and osteological elements in the autopodia of geckos, and provides evidence for associations between specific osteological traits and preferred locomotor habit. Specifically, nonclimbers exhibit longer ultimate and penultimate phalanges of Digit V in the manus and pes and also a longer fifth metatarsal in comparison with climbers, a pattern discussed here in the context of the differential demands made upon locomotion in specific ecological contexts. Our study highlights the relevance of osteological information for discussing the evolution of ecological associations of the tetrapod autopodium. J. Morphol. 278:290–299, 2017. © 2017 Wiley Periodicals, Inc.     

Patterns of morphological integration in the appendicular skeleton of mammalian carnivores

We investigated patterns of evolutionary integration in the appendicular skeleton of mammalian carnivores. The findings are discussed in relation to performance selection in terms of organismal function as a potential mechanism underlying integration. Interspecific shape covariation was quantified by two‐block partial least‐squares (2B‐PLS) analysis of 3D landmark data within a phylogenetic context. Specifically, we compared pairs of anatomically connected bones (within‐limbs) and pairs of both serially homologous and functional equivalent bones (between‐limbs). The statistical results of all the comparisons suggest that the carnivoran appendicular skeleton is highly integrated. Strikingly, the main shape covariation relates to bone robustness in all cases. A bootstrap test was used to compare the degree of integration between specialized cursorial taxa (i.e., those whose forelimbs are primarily involved in locomotion) and noncursorial species (i.e., those whose forelimbs are involved in more functions than their hindlimb) showed that cursors have a more integrated appendicular skeleton than noncursors. The findings demonstrate that natural selection can influence the pattern and degree of morphological integration by increasing the degree of bone shape covariation in parallel to ecological specialization.     

Studies of primate protein variation and evolution: Microelectrophoretic detection

Genetic variation at 16 protein and enzyme loci in Cercopithecus aethiops and several other primate species has been surveyed, using cellulose acetate microelectrophoresis. Resolution of several standard variant proteins is comparable to that achieved on starch gel or polyacrylamide gel. Although both intraspecific and interspecific variation was observed for some loci, the data generally support the concept that extracellular proteins are more likely to be polymorphic within a species, while intracellular proteins generally vary between species, if at all. These methodologies are particularly appropriate for screening multiple-locus variation in large numbers of samples; their relevance to studies of molecular evolution and evaluation of theories of kin selection is discussed.This research was supported in part by California State Agricultural Experiment Station Funds to the University of California, Berkeley, and the Wenner Gren Foundation.     

Form in the context of function: Fundamentals of an energy effective striding walk,the role of the plantigrade foot and its expected size

What morphological and functional factors allow for the unique and characteristic upright striding walk of the hominin lineage? Predictive models of locomotion that arise from considering mechanisms of energy loss indicate that collision-like losses at the transition between stance limbs are important determinants of bipedal gait. Theoretical predictions argue that these collisional losses can be reduced by having “functional extra legs” which are physically the heel and the toe part of a single anatomical foot. The ideal spacing for these “functional legs” are up to a quarter of a stride length, depending on the model employed. We evaluate the foot in the context of the dynamics of a bipedal system and compare predictions of optimal foot size against empirical data from modern humans, the Laetoli footprint trackways, and chimpanzees walking bipedally. The dynamics-based modeling approach provides substantial insight into how, and why, walking works as it does, even though current models are too simple to make predictions at a level adequate to anticipate specific morphology except at the most general level.     

Salient features in the locomotion of proboscideans revealed via the differential scaling of limb long bones

The standard differential scaling of proportions in limb long bones (length against circumference) was applied to a phylogenetically wide sample of the Proboscidea, Elephantidae and the Asian (Elephas maximus) and African (Loxodonta africana) elephants. In order to investigate allometric patterns in proboscideans and terrestrial mammals with parasagittal limb kinematics, the computed slopes between long bone lengths and circumferences (slenderness exponents) were compared with published values for mammals, and studied within a framework of the theoretical models of long bone scaling under gravity and muscle forces. Limb bone allometry in E. maximus and the Elephantidae is congruent with adaptation to bending and/or torsion induced by muscular forces during fast locomotion, as in other mammals, whereas the limb bones in L. africana appear to be adapted for coping with the compressive forces of gravity. Hindlimb bones are therefore more compliant than forelimb bones, and the resultant limb compliance gradient in extinct and extant elephants, contrasting in sign to that of other mammals, is shown to be a new important locomotory constraint preventing elephants from achieving a full‐body aerial phase during fast locomotion. Moreover, the limb bone pattern of African elephants, indicating a noncritical bone stress not increasing with increments in body weight, explains why their mean and maximal body masses are usually above those for Asian elephants. Differences in ecology may be responsible for the subtle differences observed in vivo between African and Asian elephants, but they appear to be more pronounced when revealed via mechanical patterns dictated by limb bone allometry. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 100 , 16–29.     

Exploring sexual dimorphism of human occipital and temporal bones through geometric morphometrics in an identified Western-European sample

Sex estimation is a paramount step of bioprofiling in both forensic anthropology and osteoarchaeology. When the pelvis is not optimally preserved, anthropologists commonly rely on the cranium to accurately estimate sex. Over the last decades, the geometric morphometric (GM) approach has been used to determine sexual dimorphism of the crania, in size and shape, overcoming some difficulties of traditional visual and metric methods. This article aims to investigate sexual dimorphism of the occipital and temporal region through GM analysis in a metapopulation of 50 Western-European identified individuals. Statistical analyses were performed to compare centroid size and shape data between sexes through the examination of distinct functional modules. Regression and Procrustes ANOVA were used to examine allometric and asymmetrical implications. Discriminant functions, combining size and shape data, were established. Significant dimorphism in size was found, with males having larger crania, confirming the major influence size has on cranial morphology. Allometric relationships were found to be statistically significant in both right and left temporal bones while shape differences between sexes were only significant on the right temporal bone. The visualization of the mean consensus demonstrated that males displayed a larger mastoid process associated with a reduced mastoid triangle and less projected occipital condyles. This exploratory study confirms that GM analysis represents an effective way to quantitatively capture shape of dimorphic structures, even on complex rounded ones such as the mastoid region. Further examination in a larger sample would be valuable to design objective visualization tools that can improve morphoscopic sex estimation methods.     

Locomotor behavior of wild orangutans (Pongo pygmaeus wurmbii) in disturbed peat swamp forest, Sabangau, Central Kalimantan, Indonesia

This study examined the locomotor behavior of wild Bornean orangutans (P. p. wurmbii) in an area of disturbed peat swamp forest (Sabangau Catchment, Indonesia) in relation to the height in the canopy, age-sex class, behavior (feeding or traveling), and the number of supports used to bear body mass. Backward elimination log-linear modeling was employed to expose the main influences on orangutan locomotion. Our results showed that the most important distinctions with regard to locomotion were between suspensory and compressive, or, orthograde (vertical trunk) and pronograde (horizontal trunk) behavior. Whether orangutans were traveling or feeding had the most important influence on locomotion whereby compressive locomotion had a strong association with feeding, suspensory locomotion had a strong association with travel in the peripheral strata using multiple supports, whereas vertical climb/descent and oscillation showed a strong association with travel on single supports in the core stratum. In contrast to theoretical predictions on positional behavior and body size, age-sex category had a limited influence on locomotion. The study revealed that torso orthograde suspension dominates orangutan locomotion, concurring with previous studies in dipterocarp forest. But, orangutans in the Sabangau exhibited substantially higher frequencies of oscillatory locomotion than observed at other sites, suggesting this behavior confers particular benefits for traversing the highly compliant arboreal environment typical of disturbed peat swamp forest. In addition, torso pronograde suspensory locomotion was observed at much lower levels than in the Sumatran species. Together these results highlight the necessity for further examination of differences between species, which control for habitat.     

Computed tomography and biomechanical analysis of fossil long bones.

Computerized transverse axial scanning (computed tomography) is a relatively new radiographic technique designed to recover precise cross-sectional images (tomograms) of 3-dimensional objects. This highly sensitive process permits tissues of similar density to be separated and displayed unambiguously. These special features are, therefore, ideal for analyzing the cross-sectional geometry of intact fossil long bones, even when they are highly mineralized and their medullary cavities are occluded by matrix. In order to demonstrate the utility of this method in assessing the complex relationship between fossil structure and probable function, geometrical and biomechanical properties of midshaft tomograms of femora and tibiae have been analyzed for a comparative primate sample consisting of Megaladapis edwardsi (an extinct giant prosimian from Madagascar), Indri indri (the largest extant prosimian), and Homo sapiens.     

Scaling of the limb long bones to body mass in terrestrial mammals

Long‐bone scaling has been analyzed in a large number of terrestrial mammals for which body masses were known. Earlier proposals that geometric or elastic similarity are suitable as explanations for long‐bone scaling across a large size range are not supported. Differential scaling is present, and large mammals on average scale with lower regression slopes than small mammals. Large mammals tend to reduce bending stress during locomotion by having shorter limb bones than predicted rather than by having very thick diaphyses, as is usually assumed. The choice of regression model used to describe data samples in analyses of scaling becomes increasingly important as correlation coefficients decrease, and theoretical models supported by one analysis may not be supported when applying another statistical model to the same data. Differences in limb posture and locomotor performance have profound influence on the amount of stress set up in the appendicular bones during rigorous physical activity and make it unlikely that scaling of long bones across a large size range of terrestrial mammals can be satisfactorily explained by any one power function. J. Morphol. 239:167–190, 1999. © 1999 Wiley‐Liss, Inc.     

Effects of brain and facial size on basicranial form in human and primate evolution

Understanding variation in the basicranium is of central importance to paleoanthropology because of its fundamental structural role in skull development and evolution. Among primates, encephalisation is well known to be associated with flexion between midline basicranial elements, although it has been proposed that the size or shape of the face influences basicranial flexion. In particular, brain size and facial size are hypothesized to act as antagonists on basicranial flexion. One important and unresolved problem in hominin skull evolution is that large-brained Neanderthals and some Mid-Pleistocene humans have slightly less flexed basicrania than equally large-brained modern humans. To determine whether or not this is a consequence of differences in facial size, geometric morphometric methods were applied to a large comparative data set of non-human primates, hominin fossils, and humans (N = 142; 29 species). Multiple multivariate regression and thin plate spline analyses suggest that basicranial evolution is highly significantly influenced by both brain size and facial size. Increasing facial size rotates the basicranium away from the face and slightly increases the basicranial angle, whereas increasing brain size reduces the angles between the spheno-occipital clivus and the presphenoid plane, as well as between the latter and the cribriform plate. These interactions can explain why Neanderthals and some Mid-Pleistocene humans have less flexed cranial bases than modern humans, despite their relatively similar brain sizes. We highlight that, in addition to brain size (the prime factor implicated in basicranial evolution in Homo), facial size is an important influence on basicranial morphology and orientation. To better address the multifactorial nature of basicranial flexion, future studies should focus on the underlying factors influencing facial size evolution in hominins.     

Body size and allometric variation in facial shape in children

Objectives

In group‐living primates, it has been reported that the alpha male exhibits high concentrations of cortisol and testosterone in the context of mating competition. We investigated how the presence of females affected salivary cortisol and testosterone levels in males from a small captive group of chimpanzees (Pan troglodytes). Specifically, we assessed whether the presence of females resulted in a rapid increase in salivary cortisol and testosterone levels in the alpha male.

Materials and methods

We compared the social behavior and salivary hormone concentrations of four males before and after the presentation of receptive females. Three times a day, we collected saliva samples, a useful matrix for investigating short‐term hormonal changes, and measured cortisol and testosterone concentration by liquid chromatography–tandem mass spectrometry (LC–MS/MS).

Results

The frequency of inter‐male aggression increased in the presence of females, indicating intense competition among males. Salivary cortisol levels increased in all males in the presence of females; however, the increase was significantly more pronounced in the alpha male. We found a complex three‐way interaction among the presence of females, sampling timings, and male dominance rank in the analysis of salivary testosterone. Contrary to our prediction, a post hoc analysis revealed that salivary testosterone levels decreased after female introduction and that the alpha male did not show a higher level of salivary testosterone.

Conclusions

Our study provides experimental evidence suggesting that the presence of females plays a significant role in the rank‐related variation in the cortisol levels in male chimpanzees. Furthermore, our findings demonstrate the usefulness of salivary hormones for detecting short‐term physiological changes in studies of socioendocrinology.