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.

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.

Dental microwear textural analysis as an analytical tool to depict individual traits and reconstruct the diet of a primate.

OBJECTIVES: Dental microwear is a promising tool to reconstruct animals' diet because it reflects the interplay between the enamel surface and the food items recently consumed. This study examines the sources of inter-individual variations in dietary habits in a free-ranging population of mandrills (Mandrillus sphinx) using a combination of feeding monitoring and in vivo dental microwear textural analysis (DMTA). METHODS: We investigated the impact of seasonality and individual traits on four DMTA parameters. In parallel, we further studied the influence of the physical properties of the food items consumed on these four parameters, using three proxies (mechanical properties, estimates of phytolith and external grit contents). RESULTS: We found that seasonality, age, and sex all impact DMTA parameters but those results differ depending on the facet analyzed (crushing vs. shearing facets). Three DMTA parameters (anisotropy, complexity, and heterogeneity of complexity) appear sensitive to seasonal variations and anisotropy also differs between the sexes while textural fill volume tends to vary with age. Moreover, the physical properties of the food items consumed vary seasonally and also differ depending on individual sex and age. CONCLUSION: Considering the interplay between the tested variables and both dental microwear and diet, we reaffirm that food physical properties play a major role in microwear variations. These results suggest that DMTA parameters may provide valuable hints for paleoecological reconstruction using fragmentary fossil dental remains.

Buccal dental microwear texture and catarrhine diets.

OBJECTIVES: Two-dimensional dental microwear analyses on occlusal and nonocclusal enamel surfaces have been widely applied to reconstruct the feeding behaviors of extant primates and to infer ecological adaptations in fossil hominins. To date, analyses of dental microwear texture, using three-dimensional, Scale-Sensitive Fractal Analysis approaches has only been applied to occlusal surfaces. Here, for the first time, we apply this 3D proxy to buccal enamel surfaces of catarrhine primates of known feeding ecologies to assess the utility of nonocclusal microwear texture variables as indicators of dietary habits. MATERIALS AND METHODS: Buccal microwear texture attributes were collected from high-resolution second molar casts in a sample of seven extant African catarrhine taxa with differing dietary behaviors. A white-light confocal microscope with a 100× objective lens was used to record six microwear texture variables that assess complexity, anisotropy, heterogeneity, and textural fill volume. RESULTS: The physical properties and variation in hardness of ingested foods is reflected by significant differences in the microwear variables on buccal enamel surfaces between species, which is in agreement with early reports using 2D microwear signatures of the same samples. Species that consume hard brittle items showed high buccal enamel complexity and low anisotropy values, while folivorous species that consume tough foods revealed high anisotropy and low complexity enamel patterns. DISCUSSION: Buccal microwear texture analysis on enamel surfaces clearly reflects diet-related variation in nonhuman primates. Our findings indicate that microwear texture attributes on nonworking enamel surfaces provide an alternative procedure for reconstructing dietary behavior when wear facets on occlusal surfaces are lacking.

Molar shape variability in platyrrhine primates.

Recent phylogenetic analyses suggest that platyrrhines constitute a monophyletic group represented by three families: Cebidae, Atelidae, and Pitheciidae. Morphological variability between and within these three families, however, is widely discussed and debated. The aim of this study was to assess molar shape variability in platyrrhines, to explore patterns of interspecific variation among extant species, and to evaluate how molar shape can be used as a taxonomic indicator. The analyses were conducted using standard multivariate analyses of geometric morphometric data from 802 platyrrhine lower molars. The results indicated that the interspecific variation exhibited a highly homoplastic pattern related to functional adaptation of some taxa. However, phylogeny was also an important factor in shaping molar morphological traits, given that some phenotypic similarities were consistent with current phylogenetic positions. Our results show that the phylogenetic and functional signals of lower molar shape vary depending on the taxa and the tooth considered. Based on molar shape, Aotus showed closer similarities to Callicebus, as well as to some Cebidae and Ateles-Lagothrix, due to convergent evolutionary trends caused by similar dietary habits, or due to fast-evolving branches in the Aotus lineage, somewhat similar to the shape of Callicebus and Cebidae.

Phylogenetic signal in molar dental shape of extant and fossil catarrhine primates.

Morphology has been widely used for inferring the phylogenies of numerous taxonomic groups. Recent molecular studies performed on extant non-human primates, however, have cast doubt on the reliability of cranial and postcranial characters for characterizing evolutionary affinities. Because molecular evidence is often not available for fossil specimens, detecting phylogenetic signals in anatomical features is of great relevance. Here we have analyzed molar (M1 and M2) crown shape by means of geometric morphometrics in a large sample of both extant and fossil Miocene catarrhine primates to detect the phylogenetic signal in molar morphometry. Results support that molar shape carries a strong phylogenetic signal, mostly at the superfamily level but also to some extent at the family level. Dietary factors, however, appear to have less influence, especially for M2. The Miocene Pliopithecoidea, Cercopithecoidea, and Hominoidea superfamilies clearly grouped according to the expected taxonomic affinities with the extant groups, although some discrepancies were found depending on the tooth considered. Our findings suggest that although molar crown shape can be used as a reliable proxy for establishing taxonomic affinities of catarrhine fossil primates with extant groups, a significant amount of interspecific variation exists, indicative of derived adaptations at the genus or species level.

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.

Dental shape variability in cercopithecoid primates: a model for the taxonomic attribution of macaques from Roman archaeological contexts.

Morphometric variation of biological structures has been widely used to determine taxonomic affinities among taxa, and teeth are especially informative for both deep phylogenetic relationships and specific ecological signals. We report 2-dimensional geometric morphometrics (GM) analyses of occlusal crown surfaces of lower molars (M1, n = 141; M2, n = 158) of cercopithecoid primate species. A 12-landmark configuration, including cusp tips and 8 points of the molar crown contour, were used to evaluate patterns of variation in lower molar shape among cercopithecoid primates and to predict the taxonomic attribution of 2 archaeological macaques from Roman time periods. The results showed that the lower molar shape of cercopithecoid primates reflects taxonomic affinities, mostly at a subfamily level and close to a tribe level. Thus, the cusp positions and crown contour were important elements of the pattern related to interspecific variation. Additionally, the archaeological specimens, attributed to Macaca sylvanus based on osteological information, were classified using the GM molar shape variability of the cercopithecoid primates studied. The results suggest that their molar shape resembled both M. sylvanus and M. nemestrina, and species attribution varied depending on the comparative sample used.

Brief communication: Short- and long-term in vivo human buccal-dental microwear turnover.

Buccal-dental microwear depends on the abrasive content of chewed foodstuffs and can reveal long-term dietary trends in human populations. However, in vivo experimental analyses of buccal microwear formation processes are scarce. Here, we report the effects of an abrasive diet on microwear rates in two adult volunteers at intervals of 8 days over a period of 1 month and document long-term turnover over 5 consecutive years in the same subjects under an ad libitum Mediterranean diet. Buccal microwear was analyzed on mandibular first molars using high-resolution replicas and scanning electron microscopy. Microwear turnover was assessed by recording the scratches lost and gained at each time point. Our results indicate that scratch formation on enamel surfaces increased with a highly abrasive diet compared to both pre-test and post-test ad libitum dietary controls. In the long-term analysis, scratch turnover was higher than expected, but no significant long-term trends in microwear density or length were observed, because microwear formation was compensated by scratch disappearance. Our results confirm that buccal microwear patterns on mandibular molars show a dynamic formation process directly related to the chewing of abrasive particles along with ingested food. In addition, the observed long-term stability of buccal microwear patterns makes them a reliable indicator of overall dietary habits.

Dental macrowear reveals ecological diversity of Gorilla spp.

Size and shape variation of molar crowns in primates plays an important role in understanding how species adapted to their environment. Gorillas are commonly considered to be folivorous primates because they possess sharp cusped molars which are adapted to process fibrous leafy foods. However, the proportion of fruit in their diet can vary significantly depending on their habitats. While tooth morphology can tell us what a tooth is capable of processing, tooth wear can help us to understand how teeth have been used during mastication. The objective of this study is to explore if differences in diet at the subspecies level can be detected by the analysis of molar macrowear. We analysed a large sample of second lower molars of Grauer's, mountain and western lowland gorilla by combining the Occlusal Fingerprint Analysis method with other dental measurements. We found that Grauer's and western lowland gorillas are characterised by a macrowear pattern indicating a larger intake of fruit in their diet, while mountain gorilla's macrowear is associated with the consumption of more folivorous foods. We also found that the consumption of herbaceous foods is generally associated with an increase in dentine and enamel wear, confirming the results of previous studies.

Age and individual foraging behavior predict tooth wear in Amboseli baboons.

Teeth represent an essential component of the foraging apparatus for any mammal, and tooth wear can have significant implications for survival and reproduction. This study focuses on tooth wear in wild baboons in Amboseli, southern Kenya. We obtained mandibular and maxillary tooth impressions from 95 baboons and analyzed digital images of replicas made from these impressions. We measured tooth wear as the percent dentine exposure (PDE, the percent of the occlusal surface on which dentine was exposed), and we examined the relationship of PDE to age, behavior, and life history variables. We found that PDE increased significantly with age for both sexes in all three molar types. In females, we also tested the hypotheses that long-term patterns of feeding behavior, social dominance rank, and one measure of maternal investment (the cumulative number of months that a female had dependent infants during her lifetime) would predict tooth wear when we controlled for age. The hypothesis that feeding behavior predicted tooth wear was supported. The percent of feeding time spent consuming grass corms predicted PDE when controlling for age. However, PDE was not associated with social dominance rank or maternal investment.

Tooth size variation related to age in Amboseli baboons.

We measured the molar size from a single population of wild baboons from Amboseli (Kenya), both females (n=57) and males (n=50). All the females were of known age; the males represented a mix of known-age individuals (n=31) and individuals with ages estimated to within 2 years (n=19). The results showed a significant reduction in the mesiodistal length of teeth in both sexes as a function of age. Overall patterns of age-related change in tooth size did not change whether we included or excluded the individuals of estimated age, but patterns of statistical significance changed as a result of changed sample sizes. Our results demonstrate that tooth length is directly related to age due to interproximal wearing caused by M2 and M3 compression loads. Dental studies in primates, including both fossil and extant species, are mostly based on specimens obtained from osteological collections of varying origins, for which the age at death of each individual in the sample is not known. Researchers should take into account the phenomenon of interproximal attrition leading to reduced tooth size when measuring tooth length for ondontometric purposes.

Buccal dental microwear variability in extant African Hominoidea: taxonomy versus ecology.

Buccal microwear patterns on teeth are good indicators of the abrasiveness of foodstuffs and have been used to trace the dietary habits of fossil species, including primates and hominids. However, few studies have addressed the variability of this microwear. The abrasiveness of dietary components depends not only on the hardness of the particles ingested, but also on the presence of dust and other exogenous elements introduced during food processing. These elements are responsible for the microwear typology observed on the enamel surfaces of primate teeth. Here we analyzed the variability of buccal microwear patterns in African Great Apes (Gorilla gorilla and Pan troglodytes), using tooth molds obtained from the original specimens held in several osteological collections. Our results suggest that ecological adaptations at subspecies or population level account for differences in microwear patterns, which are attributed to habitat and ecological conditions within populations rather than differences between species. The findings from studies on the variability of buccal dental microwear in extant species will contribute to a better understanding of extinct hominids' diet and ecology.

Morphological variation and covariation in mandibular molars of platyrrhine primates.

Molars are highly integrated biological structures that have been used for inferring evolutionary relationships among taxa. However, parallel and convergent morphological traits can be affected by developmental and functional constraints. Here, we analyze molar shapes of platyrrhines in order to explore if platyrrhine molar diversity reflects homogeneous patterns of molar variation and covariation. We digitized 30 landmarks on mandibular first and second molars of 418 extant and 11 fossil platyrrhine specimens to determine the degree of integration of both molars when treated as a single module. We combined morphological and phylogenetic data to investigate the phylogenetic signal and to visualize the history of molar shape changes. All platyrrhine taxa show a common shape pattern suggesting that a relatively low degree of phenotypic variation is caused by convergent evolution, although molar shape carries significant phylogenetic signal. Atelidae and Pitheciidae show high levels of integration with low variation between the two molars, whereas the Cebinae/Saimiriinae, and especially Callitrichinae, show greater variation between molars and trend toward a modular organization. We hypothesize that biomechanical constraints of the masticatory apparatus, and the dietary profile of each taxon are the main factors that determine high covariation in molars. In contrast, low molar shape covariation may result from the fact that each molar exhibits a distinct ecological signal, as molars can be exposed to distinct occlusal loadings during food processing, suggesting that different selective pressures on molars can reduce overall molar integration.

Buccal dental-microwear and dietary ecology in a free-ranging population of mandrills (Mandrillus sphinx) from southern Gabon.

Analyses of dental micro- and macro-wear offer valuable information about dietary adaptations. The buccal surface of the teeth does not undergo attrition, indicating that dental microwear may directly inform about food properties. Only a few studies have, however, investigated the environmental and individual factors involved in the formation of such microwear in wild animals. Here, we examine variation of buccal microwear patterns of mandibular molars in a large free-ranging population of mandrills (Mandrillus sphinx). We first explore the influence of seasonality and individual's sex, age and tooth macrowear-expressed as the percent of dentine exposure (PDE)-on six microwear variables. Second, we analyze the interplay between individual's diet and PDE. In a last analysis, we revisit our results on mandrills in the light of other primate's microwear studies. We show that the average buccal scratch length and the frequency of vertical buccal scratches are both higher during the long dry season compared to the long rainy season, while we observe the inverse relationship for disto-mesial scratches. In addition, females present more disto-mesial scratches than males and older individuals present higher scratch density, a greater proportion of horizontal scratches but a lower proportion of vertical scratches than young animals. PDE yields similar results than individual's age confirming earlier results in this population on the relationship between age and tooth macrowear. Because seasonality and individual characteristics are both known to impact mandrills' diet in the study population, our results suggest that buccal microwear patterns may inform about individual feeding strategies. Furthermore, PDE increases with the consumption of potentially abrasive monocotyledonous plants, independently of the individuals' age, although it is not affected by food mechanical properties. Finally, buccal scratch densities by orientation appear as relevant proxies for discriminating between different primate taxa.

The diet of the first Europeans from Atapuerca.

Hominin dietary specialization is crucial to understanding the evolutionary changes of craniofacial biomechanics and the interaction of food processing methods' effects on teeth. However, the diet-related dental wear processes of the earliest European hominins remain unknown because most of the academic attention has focused on Neandertals. Non-occlusal dental microwear provides direct evidence of the effect of chewed food particles on tooth enamel surfaces and reflects dietary signals over time. Here, we report for the first time the direct effect of dietary abrasiveness as evidenced by the buccal microwear patterns on the teeth of the Sima del Elefante-TE9 and Gran Dolina-TD6 Atapuerca hominins (1.2-0.8 million years ago - Myr) as compared with other Lower and Middle Pleistocene populations. A unique buccal microwear pattern that is found in Homo antecessor (0.96-0.8 Myr), a well-known cannibal species, indicates dietary practices that are consistent with the consumption of hard and brittle foods. Our findings confirm that the oldest European inhabitants ingested more mechanically-demanding diets than later populations because they were confronted with harsh, fluctuating environmental conditions. Furthermore, the influence of grit-laden food suggests that a high-quality meat diet from butchering processes could have fueled evolutionary changes in brain size.

Comparative analysis of dental enamel polyvinylsiloxane impression and polyurethane casting methods for SEM research.

Dental casting is a very common procedure for making high-quality replicas of paleo-anthropological remains. Replicas are frequently used, instead of original remains, to study both fossil and extant Primate teeth in morphological and metrical analyses. Several commercial products can be used in molds. This study analyzed SEM image resolution and enamel surface feature definition of tooth molds at various magnification levels and obtained, with both Coltène and 3M low-viscosity body polyvinylsiloxane impression, materials and polyurethane casts. Results, through comparison with the original teeth, show that both the negative molds and the positive casts are highly reliable in replicating enamel surfaces. However, positive cast quality is optimal for SEM observation only till the fourth consecutive replica from the original mold, especially at high SEM magnification levels.

Testing Dietary Hypotheses of East African Hominines Using Buccal Dental Microwear Data.

There is much debate on the dietary adaptations of the robust hominin lineages during the Pliocene-Pleistocene transition. It has been argued that the shift from C3 to C4 ecosystems in Africa was the main factor responsible for the robust dental and facial anatomical adaptations of Paranthropus taxa, which might be indicative of the consumption of fibrous, abrasive plant foods in open environments. However, occlusal dental microwear data fail to provide evidence of such dietary adaptations and are not consistent with isotopic evidence that supports greater C4 food intake for the robust clades than for the gracile australopithecines. We provide evidence from buccal dental microwear data that supports softer dietary habits than expected for P. aethiopicus and P. boisei based both on masticatory apomorphies and isotopic analyses. On one hand, striation densities on the buccal enamel surfaces of paranthropines teeth are low, resembling those of H. habilis and clearly differing from those observed on H. ergaster, which display higher scratch densities indicative of the consumption of a wide assortment of highly abrasive foodstuffs. Buccal dental microwear patterns are consistent with those previously described for occlusal enamel surfaces, suggesting that Paranthropus consumed much softer diets than previously presumed and thus calling into question a strict interpretation of isotopic evidence. On the other hand, the significantly high buccal scratch densities observed in the H. ergaster specimens are not consistent with a highly specialized, mostly carnivorous diet; instead, they support the consumption of a wide range of highly abrasive food items.

Canine length in wild male baboons: maturation, aging and social dominance rank.

Canines represent an essential component of the dentition for any heterodont mammal. In primates, like many other mammals, canines are frequently used as weapons. Hence, tooth size and wear may have significant implications for fighting ability, and consequently for social dominance rank, reproductive success, and fitness. We evaluated sources of variance in canine growth and length in a well-studied wild primate population because of the potential importance of canines for male reproductive success in many primates. Specifically, we measured maxillary canine length in 80 wild male baboons (aged 5.04-20.45 years) from the Amboseli ecosystem in southern Kenya, and examined its relationship with maturation, age, and social dominance rank. In our analysis of maturation, we compared food-enhanced baboons (those that fed part time at a refuse pit associated with a tourist lodge) with wild-feeding males, and found that food-enhanced males achieved long canines earlier than wild-feeding males. Among adult males, canine length decreased with age because of tooth wear. We found some evidence that, after controlling for age, longer canines were associated with higher adult dominance rank (accounting for 9% of the variance in rank), but only among relatively high-ranking males. This result supports the idea that social rank, and thus reproductive success and fitness, may depend in part on fighting ability mediated by canine size.

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.