Morphometrics of the anterior dentition in strepsirhine primates

Size variations in the anterior dentition were analyzed for 26 species of strepsirhine primates. The upper and lower incisor rows of strepsirhines, like those of anthropoid primates, scale isometrically with body size. Within the order Primates, strepsirhines exhibit the smallest incisors relative to body size, followed in increasing size by tarsiers, platyrrhines, and catarrhines. If the lateral teeth of the indriid toothcomb are interpreted as incisors and not canines, correlations between mandibular tooth size variables and body weight are maximized. The upper incisors of strepsirhines are extremely small and frequently widely separated, most likely to minimize occlusion with the toothcomb. Species deviations for assorted size variables of the anterior dentition generally fail to reflect functional variations in the use of the anterior teeth; some of the variables, however, do reflect taxonomic differences within the Strepsirhini. Although toothcomb size variations among extant strepsirhines are more readily interpreted in terms of gum feeding and bark scraping than they are in terms of grooming, anterior dental morphology as a whole is more easily explained by a grooming hypothesis when existing models of toothcomb origins are considered.     

Systematics and body size: implications for feeding adaptations in New World monkeys.

The relationship between body size and feeding ecology is well established for primates. It is argued that the evolutionary history of modern New World monkeys and, in particular, the path to attainment of current body size is significant in understanding the similarities and differences between dietary strategies and other ecological parameters of similar-sized monkeys. Current interpretations of New World monkey evolutionary relationships are reviewed. Based on a synthesis of available body weights and the assumption that the earliest New World monkeys weighed close to 1 kg, similar to modern Aotus and Callicebus, predicted patterns of body size change in each lineage are given. Restrictions on directions of body size change in primates are discussed, and it is shown that "Stanley's Rule" offers a good explanation for differing body size ranges in New and Old World anthropoids. Predicted ecological correlates to body size drawn from the mammalian literature are offered and tested using data on New World monkeys, which show some concurrence and several interesting departures from predicted patterns. Sexual dimorphism in body weight of New World monkey species is reviewed, based on the new summary of body weight data given.     

Is the Clavicle of Apes Long? An Investigation of Clavicular Length in Relation to Body Mass and Upper Thoracic Width

An elongated clavicle is one of the distinct features of apes and humans. It plays an important role in providing mobility as well as stability for the shoulder joints. The relative length of the clavicle is an especially important factor in limiting the range of shoulder joint excursion. It is said that among primates, Asian apes, i.e., gibbons and orang-utans, have very long clavicles. At the same time, they also have a wide upper thoracic cage, which may diminish the effective length of the clavicle. To clarify the length of the clavicle in apes, from the standpoint of the functional anatomy of the shoulder girdle, we examined clavicular length in 15 anthropoid species exhibiting various positional behaviors. The results confirm that clavicle length in Asian apes is long, and chimpanzees have a short clavicle like that of Old and New World monkeys, when scaled to body mass. The clavicular length of chimpanzees, however, is intermediate between Old World monkeys and Asian apes when scaled against thoracic width. Therefore, living apes can be grouped together, albeit just barely, by possession of a relatively long clavicle for their thoracic cage size. Interestingly, New World monkeys tend to exhibit a longer clavicle than Old World monkeys of equivalent body mass or thoracic cage width. Although it is unclear whether the ancestral condition of clavicular length in anthropoids was similar to that of living Old or New World monkeys, an elongation of clavicle was an important step toward evolution of the modern body plan of hominoids.     

Chewing on the trees: Constraints and adaptation in the evolution of the primate mandible

Chewing on different food types is a demanding biological function. The classic assumption in studying the shape of feeding apparatuses is that animals are what they eat, meaning that adaptation to different food items accounts for most of their interspecific variation. Yet, a growing body of evidence points against this concept. We use the primate mandible as a model structure to investigate the complex interplay among shape, size, diet, and phylogeny. We find a weak but significant impact of diet on mandible shape variation in primates as a whole but not in anthropoids and catarrhines as tested in isolation. These clades mainly exhibit allometric shape changes, which are unrelated to diet. Diet is an important factor in the diversification of strepsirrhines and platyrrhines and a phylogenetic signal is detected in all primate clades. Peaks in morphological disparity occur during the Oligocene (between 37 and 25 Ma) supporting the notion that an adaptive radiation characterized the evolution of South American monkeys. In all primate clades, the evolution of mandible size is faster than its shape pointing to a strong effect of allometry on ecomorphological diversification in this group.     

Distribution of enamel on the incisors of Old World monkeys

Longitudinal ground sections of 29 Old World monkey central lower incisors were studied histologically and metrically. Labiolingual incisor width tended to scale isometrically with body weight but with important deviations in relative incisor size, which appeared to be correlated with diet in accord with work by Hylander. Lower incisors of the predominantly folivorous colobine monkeys had a substantial layer of enamel on both lingual and labial aspects and consequently had blunt incisal edges. These teeth in both cercopithecins and papionins, which are omnivorous or frugivorous, had little or no enamel on the lingual aspect, resulting in sharp incisal edges. It is suggested that colobine incisors are used mainly in gripping and tearing leaves, whereas cercopithecine incisors are better adapted to cutting and scraping. Crown height showed a positive allometric relationship with overall incisor height, so that the tall incisors of papionins, especially Papio and Mandrillus, were more hypsodont than the shorter incisors of colobines and cercopithecins. This appears to be related to differences in the rates of incisor wear between the groups.     

Relationship of incisor size to diet and anterior tooth use in sympatric sumatran anthropoids

Researchers often relate anthropoid incisor size to diet and ingestive behaviors. It is suggested that primates that frequently consume large, tough foods (i.e., fruits) require large incisors to process these items. This idea has been difficult to test because of a lack of data on anterior tooth use in wild primates, and a lack of understanding concerning the relationships between food properties and ingestive behaviors. The first field study of primate ingestive behaviors has recently been completed for four species of Sumatran anthropoids: Hylobates lar, Macaca fascicularis, Pongo pygmaeus, and Presbytis thomasi [Ungar, American Journal of Physical Anthropology 95:197–219, 1994; International Journal of Primatology 16:221–245, 1995]. This paper documents both relative and absolute incisor row width differences among these taxa, and evaluates the relationships between incisor size and feeding behaviors for specific taxa. Results indicate that differences in incisor size among these species cannot all be explained by degree of frugivory, food item size, or even degree of incisor use in ingestion alone. It is therefore suggested that inferences of dietary differences based on largely or solely on differences in incisor sizes of specific fossil anthropoid taxa should be approached with caution. © 1996 Wiley-Liss, Inc.     

Rethinking incisor size and diet in anthropoids: diet, incisor wear and incisor breadth in the African apes

In a seminal study Hylander (1975) concluded that the length of the incisor row in catarrhines considered frugivores is longer relative to body mass than in those classified as folivores. Assuming that large fruits require greater incisal processing than do leaves, stems, berries, and seeds, he argued that the larger incisors of frugivores increased their resistance to wear. The present analysis examines diet, incisor wear, and incisor crown breadth in cranial samples of western lowland gorillas and chimpanzees. Incisor wear rate was assessed on the basis of the extent of incisor crown reduction observed at sequential stages of first molar wear. Incisor metrics were obtained from the unworn teeth of juveniles. Results suggest that incisor wear is greater in the more folivorous western lowland gorillas than in more frugivorous chimpanzees. Moreover, incisor crown dimensions do not differ appreciably among African apes. These findings fail to support the hypothesis that slower wear rates are associated with broader incisor crowns, and raise new questions regarding the significance of incisor row length in anthropoids.     

Chorionic gonadotropin has a recent origin within primates and an evolutionary history of selection

Chorionic gonadotropin (CG) is a critical signal in establishing pregnancy in humans and some other primates, but this placentally expressed hormone has not been found in other mammalian orders. The gene for one of its two subunits (CG beta subunit [CGbeta]) arose by duplication from the luteinizing hormone beta subunit gene (LHbeta), present in all mammals tested. In this study, 14 primate and related mammalian species were examined by Southern blotting and DNA sequencing to determine where in mammalian phylogeny the CGbeta gene originated. Bats (order Chiroptera), flying lemur (order Dermoptera), strepsirrhine primates, and tarsiers do not have a CGbeta gene, although they possess one copy of the LHbeta gene. The CGbeta gene first arose in the common ancestor of the anthropoid primates (New World monkeys, Old World monkeys, apes, and humans), after the anthropoids diverged from tarsiers. At least two subsequent duplication events occurred in the catarrhine primates, all of which possess multiple CGbeta copies. The LHbeta-CGbeta family of genes has undergone frequent gene conversion among the catarrhines, as well as periods of strong positive selection in the New World monkeys (platyrrhines). In addition, newly generated DNA sequences from the promoter of the CG alpha subunit gene indicate that platyrrhine monkeys use a different mechanism of alpha gene expression control than that found in catarrhines.     

Multivariate dental allometry in primates

Disagreement is current over the question of whether relatively large teeth in some large primates are a natural outcome of growth trends instead of an indication of intrinsic differences. A cross-primate survey of dental scaling relative to skull (and inferred body) size is given in this study, using a principal component technique to measure the multivariate growth relation between two sets of data: dental size and cranial size. Cheek teeth are strongly positively allometric in restriced taxonomic groups, especially in cercopithecoids. Conversely, the allometry drops to an almost linear proportional growth relation when variation in diet is controlled.     

Static intraspecific allometry of jaws and teeth in Cercopithecus aethiops

Adult static intraspecific allometry of jaw size and tooth area was evaluated in a sample of 100 Cercopithecus aethiops crania (50 male, 50 female). Tooth areas were calculated from mesiodistal and buccolingual measurements of all the teeth in both arcades and were scaled to four viscero-cranial measurements: bimaxillary breadth, maxillo-alveolar length, mandibular length and bigonial width. Allometric coefficients calculated for jaw dimensions alone indicate tighter viscerocranial integration in females than in males. A finding of note was that half of the variation in maxillo-alveolar length may be accounted for by variation in mandibular length: females are isometric, males negatively allometric.
A similar degree of allometric mosaicism was found when maxillary incisor size was scaled to maxillary length and width. In females, the relationship was negatively allometric, whilst incisor size in males was found to be unrelated to either. Negative allometry characterized the relationship of canine base area to jaw length in both sexes, with males additionally being positively allometric to mandibular width.
The scaling of postcanine tooth areas to jaw length was characterized by a dichotomous pattern: males showed significant mandibular integration whilst females showed only significant maxillary integration. Compensatory tooth size interaction between maxillary canine base area and the summed incisor and postcanine areas was suggested by the significant negative allometric relation between them.     

Curvature of the forelimb bones of anthropoid primates: Overall allometric patterns and specializations in suspensory species

It has previously been reported that brachiating primates, particularly gibbons, are characterized by distinctively straight forelimb long bones, yet no hypotheses have been proposed to explain why straight limb bones may be adaptive to suspensory locomotion. This study explores quantitatively the curvature of the long bones in 13 species of anthropoid primates and analyzes the functional consequences of curvature in biomechanical terms. These analyses demonstrate that, whereas the humeri of gibbons and spider monkeys are functionally less curved than those of other taxa, the ulnae of brachiators are neither more nor less curved than those of other anthropoids, and the gibbon radius is far more curved than would be predicted from body size alone. The humerus is likely significantly less curved in brachiators because of its torsion-dominated loading regime and the greatly increased stress magnitude developed in torsionally loaded curved beams. The large curvature of the radius is localized in the region of attachment of the supinator muscle. Analysis presented here of muscle mass allometry in catarrhines demonstrates that gibbons are characterized by an extremely massive supinator, and the large radial curvature is therefore most likely due to forearm muscle mechanics. This study also demonstrates that the overall pattern of limb bone curvature for anthropoids is distinct from the pattern reported for mammals as a whole. This distinctive scaling relationship may be related to the increased length of the limb bones of primates in comparison to other mammals.     

Size and shape of the mandibular condyle in primates

The relationships between the size of the articular surface of the mandibular condyle and masticatory muscle size, tooth size, diet, and biomechanical variables associated with mastication were studied by taking 12 measurements on skulls of 253 adult female anthropoid primates, including three to ten specimens from each of 32 species. In regressions of condylar length, width, or area against body weight, logarithmic transformations substantially improve the fit of the equations compared with untransformed data. There is a strong relationship between condylar measurements and body weight, with all correlations being .94 or higher. The slopes of the allometric regressions of length, width, and area of the condylar head indicate slight positive allometry with body size. Folivorous primates have smaller condyles than frugivorous primates, and colobines have smaller condyles than cebids, cercopithecines, or hominoids. When colobines are eliminated, the differences between frugivores and folivores are not significant. However, the two species with the relatively largest condyles are Pongo pygmaeus and Cercocebus torquatus, suggesting that there may be a relationship between unusually large condylar dimensions and the ability to crack hard nuts between the teeth. Cranial features having strong positive correlations with condylar dimensions include facial prognathism, maxillary incisor size, maxillary postcanine area, mandibular ramus breadth, and temporal fossa area. These data are interpreted as indicating that relatively large condyles are associated with relatively large masticatory muscles, relatively inefficient mandibular biomechanics, and a large dentition. These relationships support the growing evidence that the temporomandibular joint is a stress-bearing joint in normal function.     

Fatty acid composition of wild anthropoid primate milks

Fatty acids in milk reflect the interplay between species-specific physiological mechanisms and maternal diet. Anthropoid primates (apes, Old and New World monkeys) vary in patterns of growth and development and dietary strategies. Milk fatty acid profiles also are predicted to vary widely. This study investigates milk fatty acid composition of five wild anthropoids (Alouatta palliata, Callithrix jacchus, Gorilla beringei beringei, Leontopithecus rosalia, Macaca sinica) to test the null hypothesis of a generalized anthropoid milk fatty acid composition. Milk from New and Old World monkeys had significantly more 8:0 and 10:0 than milk from apes. The leaf eating species G. b. beringei and A. paliatta had a significantly higher proportion of milk 18:3n-3, a fatty acid found primarily in plant lipids. Mean percent composition of 22:6n-3 was significantly different among monkeys and apes, but was similar to the lowest reported values for human milk. Mountain gorillas were unique among anthropoids in the high proportion of milk 20:4n-6. This seems to be unrelated to requirements of a larger brain and may instead reflect species-specific metabolic processes or an unknown source of this fatty acid in the mountain gorilla diet.     

Testing the cranial evolutionary allometric ‘rule’ in Galliformes

Recent comparative studies have indicated the existence of a common cranial evolutionary allometric (CREA) pattern in mammals and birds, in which smaller species have relatively smaller faces and bigger braincases than larger species. In these studies, cranial allometry was tested using a multivariate regression between shape (described using landmarks coordinates) and size (i.e. centroid size), after accounting for phylogenetic relatedness. Alternatively, cranial allometry can be determined by comparing the sizes of two anatomical parts using a bivariate regression analysis. In this analysis, a slope higher or lower than one indicates the existence of positive or negative allometry, respectively. Thus, in those species that support the CREA ‘rule’, positive allometry is expected for the association between face size and braincase size, which would indicate that larger species have disproportionally larger faces. In this study, I applied these two approaches to explore cranial allometry in 83 Galliformes (Aves, Galloanserae), ranging in mean body weight from 30 g to 2.5 kg. The multivariate regression between shape and centroid size revealed the existence of a significant allometric pattern resembling CREA, whereas the second analysis revealed a negative allometry for beak size and braincase size (i.e. contrary to the CREA ‘rule’, larger galliform species have disproportionally shorter beaks than smaller galliform species). This study suggests that the presence of CREA may be overestimated when using cranium size as the standard measurement.     

Interspecific allometry of the mandible,dental arch,and molar area in anthropoid primates: Functional morphology of masticatory components

Allometric equations relating the lengths and widths of the mandible and dental arch, and of molar area, were obtained in a wide range of anthropoid primates grouped into four subsets, pongids, cercopithecids, nonmarmoset platyrrhines, and marmosets. Mandibular width is negatively allometric against length across anthropoids but cercopithecids had relatively wider mandibles than nonmarmosets of the same size class. Mandibular length relative to dental arch length was isometric within and between the four groups but dental arch width scaled negatively against all the other dimensions examined in this study, indicating a functional dissociation between the dental arcade and the bony mandible. Molar area showed various scaling patterns relative to mandibular length (isometry) and width (positive). There were no parameters that scaled positively against body weight across groups, except for molar area in cercopithecids (strongly) and nonmarmoset (moderately). Notable functional specializations include relatively long dental arches in cercopithecoids, related to large, elongate bilophodont molars, and the tendency to increase relative jaw length across the range of anthropoid sizes, reflecting negative allometry of the brain (cranial bicondylar width). We caution that various allometry and functional patterns may be masked by generalizing from broad taxonomic comparison involving a large sweep of adaptative patterns.     

On the definition of variables in studies of primate dental allometry

Cranial and dental measurements are taken on 253 adult female primates from 32 species. Regression equations are calculated to determine allometric relationships between anterior tooth size, posterior tooth size, and body size. When cranial length or skull length is used as the measure of general size, the results of the equations differ from when body weight is the reference dimension. Similarly, using different definitions of posterior tooth size (such as mandibular second molar length and maxillary postcanine area) alters results substantially. The same occurs with different definitions of anterior tooth size. It has been common in studies of primate dental allometry to generalize from the specific variables measured to broad functional interpretations. However, highly correlated variables cannot be substituted one for another in allometric analyses without important changes in the results of the equation. Interpretation of allometric data is more highly restricted to the precise variables measured in a particular study than has been generally recognized.     

The allometric pattern of sexually size dimorphic feather ornaments and factors affecting allometry

The static allometry of secondary sexual characters is currently subject to debate. While some studies suggest an almost universal positive allometry for such traits, but isometry or negative allometry for nonornamental traits, other studies maintain that any kind of allometric pattern is possible. Therefore, we investigated the allometry of sexually size dimorphic feather ornaments in 67 species of birds. We also studied the allometry of female feathers homologous to male ornaments (female ornaments in the following) and ordinary nonsexual traits. Allometries were estimated as reduced major axis slopes of trait length on tarsus length. Ornamental feathers showed positive allometric slopes in both sexes, although that was not a peculiarity for ornamental feathers, because nonsexual tail feathers also showed positive allometry. Migration distance (in males) and relative size of the tail ornament (in females) tended to be negatively related to the allometric slope of tail feather ornaments, although these results were not conclusive. Finally, we found an association between mating system and allometry of tail feather ornaments, with species with more intense sexual selection showing a smaller degree of allometry of tail ornaments. This study is consistent with theoretical models that predict no specific kind of allometric pattern for sexual and nonsexual characters.     

Allometry of facial mobility in anthropoid primates: implications for the evolution of facial expression

Body size may be an important factor influencing the evolution of facial expression in anthropoid primates due to allometric constraints on the perception of facial movements. Given this hypothesis, I tested the prediction that observed facial mobility is positively correlated with body size in a comparative sample of nonhuman anthropoids. Facial mobility, or the variety of facial movements a species can produce, was estimated using a novel application of the Facial Action Coding System (FACS). I used FACS to estimate facial mobility in 12 nonhuman anthropoid species, based on video recordings of facial activity in zoo animals. Body mass data were taken from the literature. I used phylogenetic generalized least squares (PGLS) to perform a multiple regression analysis with facial mobility as the dependent variable and two independent variables: log body mass and dummy-coded infraorder. Together, body mass and infraorder explain 92% of the variance in facial mobility. However, the partial effect of body mass is much stronger than for infraorder. The results of my study suggest that allometry is an important constraint on the evolution of facial mobility, which may limit the complexity of facial expression in smaller species. More work is needed to clarify the perceptual bases of this allometric pattern.     

Modes of ontogenetic allometric shifts in crocodylian vertebrae

During postnatal ontogeny of vertebrates, allometric trends in certain morphological units or dimensions can shift drastically among isometry, positive allometry, and negative allometry. However, detailed patterns of allometric transitions in certain timings have not been explored well. Identifying the presence and nature of allometric shifts is essential for understanding the patterns of changes in relative size and shape and the proximal factors that are controlling these changes mechanistically. Allometric trends in 10 selected vertebrae (cervical 2–caudal 2) from hatchlings to very mature individuals of Alligator mississippiensis (Archosauria, Crocodylia) are reported in the present study. Allometric coefficients in 12 vertebral dimensions are calculated and compared relative to total body length, including centrum, neural spine, transverse process, zygapophysis, and neural pedicle. During the postnatal growth, positive allometry is the most common type of relative change (10 of the 12 dimensions), although the diameter of the neural canal shows a negative allometric trend. However, when using spurious breaks (i.e. allometric trends subdivided into growth stages using certain growth events, and key body sizes and/or ages), vertebral parts exhibit various pathways of allometric shifts. Based on allometric trends in three spurious breaks, separated by the end of endochondral ossification (body length: approximnately 0.9 m), sexual maturity (1.8 m), and the stoppage of body size increase (2.8 m), six types of ontogenetic allometric shifts are established. Allometric shifts exhibit a wide range from positive allometry restricted only in the early postnatal stage (Type I) to life‐long positive allometry (Type VI). This model of ontogenetic allometric shifts is then applied to interpret potential mechanisms (causes) of allometric changes, such as (1) growth itself (when allometric trend gradually decreases to isometric or negative allometric change: Type II–IV allometric shift); (2) developmental constraint (when positive allometry is limited only in the early growth stage: Type I allometric shift); and (3) functional or biomechanical drive (when positive allometry continues throughout ontogeny: Type VI allometric shift).     

Allometric scaling in the dentition of primates and prediction of body weight from tooth size in fossils

Tooth size varies exponentially with body weight in primates. Logarithmic transformation of tooth crown area and body weight yields a linear model of slope 0.67 as an isometric (geometric) baseline for study of dental allometry. This model is compared with that predicted by metabolic scaling (slope = 0.75). Tarsius and other insectivores have larger teeth for their body size than generalized primates do, and they are not included in this analysis. Among generalized primates, tooth size is highly correlated with body size. Correlations of upper and lower cheek teeth with body size range from 0.90–0.97, depending on tooth position. Central cheek teeth (P and M) have allometric coefficients ranging from 0.57–0.65, falling well below geometric scaling. Anterior and posterior cheek teeth scale at or above metabolic scaling. Considered individually or as a group, upper cheek teeth scale allometrically with lower coefficients than corresponding lower cheek teeth; the reverse is true for incisors. The sum of crown areas for all upper cheek teeth scales significantly below geometric scaling, while the sum of crown areas for all lower cheek teeth approximates geometric scaling. Tooth size can be used to predict the body weight of generalized fossil primates. This is illustrated for Aegyptopithecus and other Eocene, Oligocene, and Miocene primates. Regressions based on tooth size in generalized primates yield reasonable estimates of body weight, but much remains to be learned about tooth size and body size scaling in more restricted systematic groups and dietary guilds.