Morphological integration affects the evolution of midline cranial base, lateral basicranium, and face across primates

Objectives The basicranium and face are two integrated bony structures displaying great morphological diversity across primates. Previous studies in hominids determined that the basicranium is composed of two independent modules: the midline basicranium, mostly influenced by brain size, and the lateral basicranium, predominantly associated with facial shape. To better assess how morphological integration impacts the evolution of primate cranial shape diversity, we test to determine whether the relationships found in hominids are retained across the order. Materials and methods Three-dimensional landmarks (29) were placed on 143 computed tomography scans of six major clades of extant primate crania. We assessed the covariation between midline basicranium, lateral basicranium, face, and endocranial volume using phylogenetically informed partial least squares analyses and phylogenetic generalized least squares models. Results We found significant integration between lateral basicranium and face and between midline basicranium and face. We also described a significant correlation between midline basicranium and endocranial volume but not between lateral basicranium and endocranial volume. Discussion Our findings demonstrate a significant and pervasive integration in the craniofacial structures across primates, differing from previous results in hominids. The uniqueness of module organization in hominids may explain this distinction. We found that endocranial volume is significantly integrated to the midline basicranium but not to the lateral basicranium. This finding underlines the significant effect of brain size on the shape of the midline structures of the cranial base in primates. With the covariations linking the studied features defined here, we suggest that future studies should focus on determining the causal links between them

Basicranium and face: Assessing the impact of morphological integration on primate evolution

The basicranium and facial skeleton are two integrated structures displaying great morphological diversity across primates. Previous studies focusing on limited taxonomic samples have demonstrated that morphological integration has a significant impact on the evolution of these structures. However, this influence is still poorly understood. A more complete understanding of craniofacial integration across primates has important implications for functional hypotheses of primate evolution. In the present study, we analyzed a large sample of primate species to assess how integration affects the relationship between basicranial and facial evolutionary pathways across the order. First, we quantified integration and modularity between basicranium and face using phylogenetically-informed partial least squares analyses. Then, we defined the influence of morphological integration between these structures on rates of evolution, using a time-calibrated phylogenetic tree, and on disparity through time, comparing the morphological disparity across the tree with that expected under a pure Brownian process. Finally, we assessed the correlation between the basicranium and face, and three factors purported to have an important role in shaping these structures during evolution: endocranial volume, positional behavior (i.e., locomotion and posture), and diet. Our findings show that the face and basicranium, despite being highly integrated, display significantly different evolutionary rates. However, our results demonstrate that morphological integration impacted shape disparity through time. We also found that endocranial volume and positional behavior are important drivers of cranial shape evolution, partly affected by morphological integration. (C) 2018 Elsevier Ltd. All rights reserved

Relationship between foramen magnum position and locomotion in extant and extinct hominoids

From the Miocene Sahelanthropus tchadensis to Pleistocene Homo sapiens, hominins are characterized by a derived anterior position of the foramen magnum relative to basicranial structures. It has been previously suggested that the anterior position of the foramen magnum in hominins is related to bipedal locomotor behavior. Yet, the functional relationship between foramen magnum position and bipedal locomotion remains unclear. Recent studies, using ratios based on cranial linear measurements, have found a link between the anterior position of the foramen magnum and bipedalism in several mammalian clades: marsupials, rodents, and primates. In the present study, we compute these ratios in a sample including a more comprehensive data set of extant hominoids and fossil hominins. First, we verify if the values of ratios can distinguish extant humans from apes. Then, we test whether extinct hominins can be distinguished from non-bipedal extant hominoids. Finally, we assess if the studied ratios are effective predictors of bipedal behavior by testing if they mainly relate to variation in foramen magnum position rather than changes in other cranial structures. Our results confirm that the ratios discriminate between extant bipeds and non-bipeds. However, the only ratio clearly discriminating between fossil hominins and other extant apes is that which only includes basicranial structures. We show that a large proportion of the inter-specific variation in the other ratios relates to changes in facial, rather than basicranial, structures. In this context, we advocate the use of measurements based only on basicranial structures when assessing the relationship between foramen magnum position and bipedalism in future studies. (C) 2017 Elsevier Ltd. All rights reserved

Considering the constrained lever model: Feeding biomechanics of OH 5 assessed using finite element analysis

The craniofacial morphology of Paranthropus boisei exhibits a number of highly derived characteristics that have been argued to be functionally related to feeding. These features are hypothesized to either decrease structural stress, increase the mechanical advantage of the masticatory muscles, or both. But complications arise when the constrained lever model is considered. This study uses finite element analysis to test the hypothesis that the P. boisei cranium is structurally stronger and configured to more efficiently generate bite force than the crania of Pan troglodytes and Australopithecus africanus. To assess our analyses within the context of the constrained lever model of chewing biomechanics, joint reaction forces are also examined. A finite element model was created from a reconstruction of the OH 5 cranium. The model was assigned chimpanzee material properties, constrained at the TMJs and bite points, and subjected to scaled muscle forces derived from chimpanzees. Strains, bite forces and strain energy were recorded. The results were compared to those from FEA of other hominid crania. Results indicate the face of P. boisei is structurally strong and the extreme morphology of this species allows for the generation of high bite forces on posterior teeth without violating the constrained lever model

Geometric morphometrics and finite element analyses reveal the Haast's eagle (Harpagornis moorei) to be a mixed predator-scavenger

The extinct Haast’s eagle (Harpagornis moorei) was 30-40% heavier than the largest extant eagle. There have been speculations about its evolutionary history and ecology, though there is still no consensus on its feeding behaviour. This study aims at understanding the evolution and ecology of Harpagornis by combining 3D geometric morphometrics and finite element analysis (FEA) on three-dimensional models constructed from CT-data of skulls and talons of Accipitridae. Statistical analyses revealed the presence of two independent modules (beak and neurocranium) and of a strong allometric effect in the skull. Size-free shape analysis of the two modules revealed that Harpagornis’ beak was similar to the eagles, while it’s neurocranial morphology was more like a vulture. In most cranial FEA loading cases, there seems to be a dichotomy between Cathartidae on the one side and Accipitridae on the other. FEA on the skull, nevertheless, indicates that Harpagornis and the scavenging species of our dataset are well adapted to perform a pull-back motion. The talon results suggest Harpagornis was an active hunter. Harpagornis’ talon occupies a position in morphospace close to its closest living relative Hieraaetus (smallest extant eagle), suggesting a phylogenetic constraint on talon shape. However, FEA showed that the talon of Harpagornis undergoes similar stresses to that of other hunting raptors which rely on large-sized prey (e.g. Aquila audax). Neurocranial morphology and FEA, however, clearly indicate a feeding behaviour more similar to vultures, possibly because of the large size of its prey (e.g., giant Moa). Harpagornis’ neurocranial adaptation probably allowed a stronger and faster pull back motion to quickly remove large chunks of meat from the prey, similarly to vultures. Moreover, our results document a rapid evolutionary change, which might have allowed Harpagornis to exploit large sized prey. Harpagornis moorei therefore represents an extreme example of how freedom from competition in island ecosystems can rapidly influence morphological adaptation

Age-Related Tooth Wear Differs between Forest and Savanna Primates

Tooth wear in primates is caused by aging and ecological factors. However, comparative data that would allow us to delineate the contribution of each of these factors are lacking. Here, we contrast age-dependent molar tooth wear by scoring percent of dentine exposure (PDE) in two wild African primate populations from Gabonese forest and Kenyan savanna habitats. We found that forest-dwelling mandrills exhibited significantly higher PDE with age than savanna yellow baboons. Mandrills mainly feed on large tough food items, such as hard-shell fruits, and inhabit an ecosystem with a high presence of mineral quartz. By contrast, baboons consume large amounts of exogenous grit that adheres to underground storage organs but the proportion of quartz in the soils where baboons live is low. Our results support the hypothesis that not only age but also physical food properties and soil composition, particularly quartz richness, are factors that significantly impact tooth wear. We further propose that the accelerated dental wear in mandrills resulting in flatter molars with old age may represent an adaptation to process hard food items present in their environment