Dental eruption sequence among colobine primates

Dental development is one aspect of growth that is linked to diet and to life history but has not been investigated among colobines since the work of Schultz [1935]. This study establishes the dental eruption sequence for several colobine species and compares it to that of other catarrhines. The mandibles and maxillae of two hundred and four juvenile colobine specimens were scored for presence or absence of permanent teeth and for stages of partial eruption. Eruption was defined as ranging between tooth emergence (any part of a tooth crown above the alveolar margin) and full occlusion, with three intermediate levels manifest between these boundaries. In African colobines, represented by C. guereza, C. angolensis and P. badius, M2 erupts before I2, and in C. angolensis it also erupts before I1. The canine is delayed, erupting after the premolars in females and after M3 in males. Asian colobines show greater diversity in eruption sequences. Nasalis shows no early eruption of the molars and is very similar to Macaca. In Trachypithecus and Pygathrix M(2) erupts before I(2). The canine in Trachypithecus is delayed, erupting after the premolars and, in some males, after M3. In Presbytis M2 erupts before both incisors; M3 erupts before C in both sexes, and often before both premolars. Although the actual timing of eruption is unknown, all colobine species examined except N. larvatus showed some degree of relatively early eruption of M2 and M3. The lack of this tendency in Nasalis sets this genus apart from all other colobines represented in this study. Dental eruption sequence is thought to reflect life history patterns. Early molar eruption in colobines was thought by Schultz (1935) to be a primitive character reflecting shorter life history. Faster growth rates found in folivorous primates have been interpreted as being related to an adaptation to folivory (Leigh 1994), and early eruption of molars may be part of this dietary specialization. The relationships between dental development and both diet and life history are investigated.     

Relationships between the fossil colobine Mesopithecus pentelicus and extant cercopithecoids, based on dental metrics

Maxillary dental measurements from six specimens of Mesopithecus pentelicus, 64 cercopithecines, 59 African colobines, and 64 Asian colobines were analyzed by means of a "nested research design" that was specifically designed to explore the affiliation between fossils and extant cercopithecoids at different systematic levels. The results showed that the variation among taxonomic groups was mainly associated with size; however, in addition, interesting shape differences emerged, molars were shown to be important discriminators, Mesopithecus was confirmed as a colobine (as expected) and found to be closer to Asian species than to African ones, and the odd-nosed colobines were found to share more dental similarities with Mesopithecus than other colobines. The last finding is in contrast to previous studies, in which it was proposed that M. pentelicus is morphologically closely related to the African colobus and the gray langur (Semnopithecus).     

Dental Eruption Sequences in Fossil Colobines and the Evolution of Primate Life Histories

Unlike other catarrhines, colobines show early molar eruption relative to that of the anterior dentition. The pattern is variable, with Asian genera (Presbytina) showing a greater variability than the African genera (Colobina). The polarity of early relative molar eruption, as well as the degree to which it is related to phylogeny, are unclear. Schultz (1935) suggested that the trend reflects phylogeny and is primitive for catarrhines. More recently, however, researchers have proposed that life history and dietary hypotheses account for early relative molar eruption. If the colobine eruption pattern is primitive for catarrhines, it implies that cercopithecines and hominoids converged on delayed relative molar eruption. Alternatively, if the colobine condition is derived, factors such as diet and mortality patterns probably shaped colobine eruption patterns. Here we update our knowledge on eruption sequences of living colobines, and explore the evolutionary history of the colobine dental eruption pattern by examining fossil colobine taxa from Eurasia (Mesopithecus) and Africa (Kuseracolobus aramisi and Colobus sp.) and the basal cercopithecoid Victoriapithecus macinnesi. We scored specimens per Harvati (2000). The Late Miocene-Early Pliocene Mesopithecus erupts the second molar early relative to the incisors, while the Early Pliocene Kuseracolobus aramisi does not. These results demonstrate that the common colobine tendency for early molar eruption relative to the anterior dentition had appeared by the Late Miocene, and that some of the diversity observed among living colobines was already established in the Late Miocene/Early Pliocene. We discuss the implications of these results for phylogenetic, life history, and dietary hypotheses of dental development.     

Underbite and the scaling of facial dimensions in colobine monkeys.

This investigation was concerned with the dimensions of the facial skeleton and the incidence of underbite in colobine monkeys. Standard craniofacial dimensions and the notation of the presence or absence of underbite were recorded for skulls of 308 adult, wild-caught colobines belonging to 10 species. Underbite was noted in all species examined, ranging in frequency from 10% in Colobus polykomos to 100% in 2 species of Presbytis. Univariate statistics indicate that species with high frequencies of underbite tend to have shorter, broader maxillary dental arches, shorter faces and rostrums, and longer mandibular dental arches. A multivariate discriminant analysis supported the univariate statistics. Interspecific allometric analysis of facial measurements against a constructed size variable indicated that maxillary dimensions scale in a strongly positive manner in relation to size. However, mandibular dimensions tend to scale isometrically. This pattern of facial scaling indicates that the tendency toward underbite should increase as overall size decreases. This would explain why smaller species have higher frequencies of underbite than larger species and why females often have a higher incidence of underbite than conspecific males. Zingeser has suggested that the high incidence of underbite in colobine and some cebid monkeys is an adaptation to folivory. The results of this study support an alternative hypothesis that the high incidence of underbite in colobine monkeys is related to the pattern of facial scaling with size in combination with relaxed selection on the anterior dentition.     

Dental reductions and dental caries

Although first permanent molar hypoconulid absence, third molar agenesis, and small tooth size are all part of the evolutionary trend of dental reduction, each bears a different relationship to dental caries. Caries prevalence in the maxillary and mandibular permanent first molars of the Burlington Research Centre serial experimental group at age 16 years was less in the children whose first molars were missing the hypoconulid. Conversely, caries prevalence in mandibular first molars was greater in the children who had agenesis of third molars. The extraction of first molars due to caries was more frequent in children with agenesis of third molars, less frequent in those with absence of hypoconulids of the first molars and unrelated to tooth size. Caries prevalence was less in small teeth, and occurred least in the small mandibular first molars with four cusps. Whereas this is in harmony with the hypothesis that evolutionary dental reductions resulted from the pressure of caries, the increased prevalence of caries and extractions coinciding with third molar agenesis does not support this view. In addition, agenesis of hypoconulids and agenesis of third molars were related to changes in structures unrelated to caries.     

Craniodental mechanics and diet in Asian colobines: Morphological evidence of mature seed predation and sclerocarpy

Folivory has been accepted as the general dietary pattern for colobines. However, recent ecological studies have revealed that extensive seed eating is found in some colobine species. The ripeness of foraged seeds is also reported to differ between seed eaters. As seeds are generally stress‐limited and may pose greater mechanical demands, seed‐eating species are predicted to exhibit morphological features adaptive for seed predation. In addition, species that feeds on seeds from unripe fruits with hard pericarp is predicted to exhibit increased leverage for anterior dentition. To test these hypotheses, we compared the craniodental morphology of seed‐eating Asian colobines (Presbytis rubicunda and Trachypithecus phayrei) with those of species that rarely exploit seeds (Presbytis comata, Trachypithecus obscurus, and Semnopithecus vetulus). The results show that the seed‐eating colobines possess a masticatory system with enhanced leverage at postcanine bite points. The sclerocarpic forager P. rubicunda also exhibits markedly greater masticatory leverage at anterior dental bite points, while the mature‐seed‐eating T. phayrei shows no such advantage for canine and incisor use. These observations suggest that P. rubicunda is well adapted to husking the resistant pericarps of unripe fruits, using the anterior dentition and to gain access to the immature seeds, whereas such sclerocarpic feeding behavior may be less important for T. phayrei. Our findings indicate that the distinctive craniodental variations of colobines may be linked to mature and/or immature seed eating and suggest the significance of seed predation for the evolution of colobine monkeys. Am J Phys Anthropol, 2010. © 2010 Wiley‐Liss, Inc.     

Systematic classification of Asian colobines

In order to study the differentiation of Asian colobines, fourteen variables were analysed in one way, on 123 skulls, includingRhinopithecus, Presbytis, Presbytiscus, Pygathrix, andNasalis with both cluster and differentiated functions tests. Information on paleoenvironment changes in China and South-East Asia since late Tertiary have been used to examine the influences of migratory habits and the distribution range in Asian colobines. The cladogram among different Asian colobines genera was made from the results of various analysis. Some new points or revisions were suggested: 1. Following the second migratory way, ancient species of Asian colobines perhaps passed through Xizang along the northern bank of Tethis sea and Heng-Duan Shan regions, across Yunnan into Vietnam, since the ancient continent between Yunnan and Xizang was already located in on eastern bank of Tethis sea. Thus, during the evolution, Asian colobines must have had two original centres, i.e. “Sundaland” and Heng-Duan Shan Chinese regions; 2. Pygatrix possesses a lot of cranial features more similar toPresbytiscus than toRhinopithecus. The small difference from the modification combinesPygatrix with other two genera as shown by Groves (1970), but it is better to putPygatrix andPresbytiscus together as one genus; 3.Nasalis (2n=48) may be the most primitive genus within Asian colobines. Some features shared withRhinopithecus, for example body size, terrestrial activities, limb proportion etc. ...seem to be considered as a common inheritance of symlesiomorphus characters; 4.Rhinopithecus, with reference to cranioface and cranium or to its origin, is a special genus of Asian colobine. It may represent the highest level of evolutionary position within various genera (Peng et al., 1985).     

Mapping homology between human and black and white colobine monkey chromosomes by fluorescent in situ hybridization

We used in situ hybridization of chromosome specific DNA probes (“chromosome painting”) of all human chromosomes to establish homologies between the human and the white and black colobus (Colobus guereza 2n = 44). The 24 human paints gave 31 signals on the autosomes (haploid male chromosome set). Robertsonian translocations between chromosomes homologus to human 14 and 15, 21 and 22, form colobine chromosomes 6 and 16, respectively. Reciprocal translocations were found between human chromosomes 1 and 10, 1 and 17, as well as 3 and 19. The alternating hybridization signals between human 3 and 19 on Colobus chromosome 12 show that in this case a reciprocal translocation was followed by a pericentric inversion. The hybridization data show that in spite of the same diploid number and similar Fundamental Numbers, the black and white colobine monkey differs from Presbytis cristata, an Asian colobine, by 6 reciprocal translocations. Comparisons with the hybridization patterns in other primates show that some Asian colobines have a more derived karyotype with respect to African colobines, macaques, great apes, and humans. Chromosome painting also clearly shows that similarities in diploid number and chromosome morphology both between colobines and gibbons are due to convergence. Am. J. Primatol. 42:289–298, 1997. © 1997 Wiley-Liss, Inc.     

Brief communication: Identification reassessment of the isolated tooth Krapina D58 through occlusal fingerprint analysis

High variability in the dentition of Homo can create uncertainties in the correct identification of isolated teeth. For instance, standard tooth identification criteria cannot determine with absolute certainty if an isolated tooth is a second or third maxillary molar. In this contribution, using occlusal fingerprint analysis, we reassess the identification of Krapina D58 (Homo neanderthalensis), which is catalogued as a third maxillary molar. We have hypothesized that the presence/absence of the distal occlusal wear facets can be used to differentiate second from third maxillary molars. The results obtained confirm our hypothesis, showing a significant difference between second and third maxillary molars. In particular we note the complete absence of Facets 7 and 10 in all third molars included in this analysis. The presence of these facets in Krapina D58 eliminates the possibility that it is a third maxillary molar. Consequently it should be reclassified as a second molar. Although this method is limited by the degree of dental wear (i.e., unworn teeth cannot be analyzed) and to individual molars in full occlusion, it can be used for tooth identification when other common criteria are not sufficient to discriminate between second and third maxillary molars. Am J Phys Anthropol 143:306–312, 2010. © 2010 Wiley‐Liss, Inc.     

亚洲疣猴与猕猴牙齿的比较

为了研究亚洲疣猴牙齿形态与功能适应性之间的关系,建立异速生长公式比较分析生活于同一大陆的猕猴。主成份分析用来分析来自异速生长公式的残差。结果表明:疣猴出乎意料地展示了比猕猴更小的门齿。导致此结果的可能原因是:疣猴与猕猴之间的食物差异性。但是,这种差异小于亚-非大陆种类。也就是说,在过去的500万年左右的时间里,生活于同一大陆的疣猴和猕猴已经产生了一些对环境和食性的趋同性。当每一个疣猴属分别与猕猴进行比较时,它们之间的差异性揭示了地理分布的差异。金丝猴(Rhinopithecus)和长尾叶猴(Semnopithecus)具有比其他疣猴发达的臼齿。欧氏距离的结果说明疣猴和猕猴牙齿的差异性揭示了它们在系统发育方面的关系。     

亚洲疣猴面颅和脑颅的比较研究

对亚洲疣猴123个头骨的面颅和脑颅的14项变量作了分析。讨论了东亚古环境的变迁对亚洲疣猴辐射的影响。据分析结果,似乎获得了几个新结论:1)亚洲疣猴可能还有另一条迁移路线——沿特蒂斯海北岸的西藏南部进入我国横断山区,故它们可能有两个分化或辐射中心,即“Sundaland”和我国的横断山地区;2)Nasalis(2n=48)可能是亚洲疣猴中最原始的一个属;3)Pygathrix与Presbytiscus具有最大的相似性,但前者与Phinopithecus相差甚远;4)Phinopithecus无论面颅和脑颅或是起源都是亚洲疣猴中更为特化的一个属。提出了亚洲疣猴系统发育支序图。     

The Hand of Cercopithecoides williamsi (Mammalia,Primates): Earliest Evidence for Thumb Reduction among Colobine Monkeys

Thumb reduction is among the most important features distinguishing the African and Asian colobines from each other and from other Old World monkeys. In this study we demonstrate that the partial skeleton KNM-ER 4420 from Koobi Fora, Kenya, dated to 1.9 Ma and assigned to the Plio-Pleistocene colobine species Cercopithecoides williamsi, shows marked reduction of its first metacarpal relative to the medial metacarpals. Thus, KNM-ER 4420 is the first documented occurrence of cercopithecid pollical reduction in the fossil record. In the size of its first metacarpal relative to the medial metacarpals, C. williamsi is similar to extant African colobines, but different from cercopithecines, extant Asian colobines and the Late Miocene colobines Microcolobus and Mesopithecus. This feature clearly links the genus Cercopithecoides with the extant African colobine clade and makes it the first definitive African colobine in the fossil record. The postcranial adaptations to terrestriality in Cercopithecoides are most likely secondary, while ancestral colobinans (and colobines) were arboreal. Finally, the absence of any evidence for pollical reduction in Mesopithecus implies either independent thumb reduction in African and Asian colobines or multiple colobine dispersal events out of Africa. Based on the available evidence, we consider the first scenario more likely.     

Jaw morphology and function in living and fossil old world monkeys

This allometric investigation on a sample of 29 cercopithecine and 22 colobine taxa augments the data and implications of prior work on subfamilial variation in mandibular form and function in recent Cercopithecidae. To increase the size range encompassed by living cercopithecines and colobines, I included many of the larger-bodied fossil specimens. These analyses serve to fill a gap in our understanding of size-related changes in masticatory function and symphyseal morphology and curvature in extant and extinct Old World monkeys. Results of subfamilial scaling comparisons indicate that for a given jaw length, colobines possess significantly more robust corpora and symphyses than those of cercopithecines, especially at smaller sizes. Following from previous work, the most plausible explanation for why the subfamilies differ in relative corporeal and symphyseal dimensions is that colobine mandibles experience elevated loads and greater repetitive loading during mastication due, on average, to processing a diet of tough leaves and/or seeds. Although colobines have relatively larger symphyses, subfamilial analyses of symphyseal curvature demonstrate that they evince less symphyseal curvature vis-à-vis cercopithecines of a common size. Moreover, both subfamilies exhibit similar allometric changes in the degree of curvature, such that larger-bodied Old World monkeys have more curved symphyses than those of smaller taxa. Subfamilial scaling analyses also indicate that colobines possess a shorter M2 bite-point length relative to masseter lever-arm length, but not versus temporalis lever-arm length. Thus, as compared to cercopithecines, colobines can recruit less masseter-muscle force to produce similar bite forces during mastication. In both clades, M² bite-point length scales with positive allometry relative to masseter lever-arm length, such that larger species are less efficient at generating molar bite forces. This seems especially important due to the lack of subfamily difference in M² bite-point:temporalis lever-arm scaling (which is isometric across cercopithecids). A consideration of extinct cercopithecids indicates that many of the large-bodied papionins have more robust corpora, due perhaps to a diet which was of similar toughness to that of extant and extinct colobines. However, the biomechanical arrangements of the masseter and temporalis in all but one fossil cercopithecine and all of the fossil colobine specimens are much as predicted for a subfamilial member of its skull size. That most large-bodied papionins with tougher diets nonetheless maintain a less efficient jaw-muscle configuration may be due to stronger offsetting selection for increased relative canine size and gape.     

Brief communication: correcting overestimation when determining two-dimensional occlusal area in human molars

The robustness index (RI) is determined by multiplying dental mesiodistal and buccolingual diameters, and is used to estimate occlusal area. However, because teeth are not rectangular its calculation consistently causes overestimations. Moreover, teeth, in particular molars, are not identically shaped so overestimations vary. The current study seeks to determine the extent to which overestimations are affected by tooth shape and to improve RI's efficacy. Initially, 120 molars were sorted into six shape groups, which were determined by hypocone/hypoconulid expression. Three maxillary and three mandibular shape groups were set using the Arizona State University Dental Anthropology System. ANOVA results determined that RI overestimations, which averaged around 20%, were not the same for each shape category. Maxillary molars with large hypocones and mandibular molars with no hypoconulids were overestimated significantly less than the other molar groups. Regression-based correction formulae were generated and applied to the original sample. These formulae far more precisely estimated tooth area than RI and there were no differences in estimation based upon tooth shape. A subsequent validation study of 24 additional molars was undertaken to test the formulae on teeth not from the original sample. Overestimation/underestimation averaged 0.5% and was about the same for each of the tooth shape groups. Finally, six new correction formulae were generated using all 144 molars. The correction formulae provide, what is termed here, an adjusted robustness index (ARI), and it is recommended that ARI is used in future studies of molar occlusal area.     

Mitochondrial data support an odd-nosed colobine clade

To obtain a more complete understanding of the evolutionary history of the leaf-eating monkeys we have examined the mitochondrial genome sequence of two African and six Asian colobines. Although taxonomists have proposed grouping the "odd-nosed" colobines (proboscis monkey, douc langur, and the snub-nosed monkey) together, phylogenetic support for such a clade has not been tested using molecular data. Phylogenetic analyses using parsimony, maximum likelihood, and Bayesian methods support a monophyletic clade of odd-nosed colobines consisting of Nasalis, Pygathrix, and Rhinopithecus, with tentative support for Nasalis occupying a basal position within this clade. The African and Asian colobine lineages are inferred to have diverged by 10.8 million years ago (mya or Ma). Within the Asian colobines the odd-nosed clade began to diversify by 6.7 Ma. These results augment our understanding of colobine evolution, particularly the nature and timing of the colobine expansion into Asia. This phylogenetic information will aid those developing conservation strategies for these highly endangered, diverse, and unique primates.     

Perinatal dental development in the chimpanzee (Pan troglodytes)

The synthesis of both ontogenetic and phylogenetic data should provide the ideal explanation of morphologic variation, but for the primate dentition, this has not yet occurred. Information concerning growth and development of primate teeth is lacking, in part because of the paucity of specimens. We have therefore examined the deciduous second molars (dm2) and tooth buds of the permanent first molar (M1) of 12 chimpanzees (Pan troglodytes), aged 6.5 months of gestation to 4 postnatal months. The ordering of cusp calcification was identical to that of other primates. By regression analysis, correlations of mesial and distal widths with buccal, lingual, and mesiodistal lengths were low, most probably because of decreased rates of change (slopes) and the relatively small sample size. Correlations were, however, greater for mandibular than for maxillary dentition and higher for age than for body weight; for both the dm2 and M1, distal moieties increased faster and were more highly correlated with other dental variables and age than were mesial ones. Comparison with data from humans revealed both differences and similarities in the absolute size and growth rate of dental moieties during the perinatal period. As the reasons for ontogenetic variation become understood for individuals, species, and higher taxa, the phylogenetic implications of differential growth should become clearer as well.     

Variation in hominoid molar enamel thickness

Enamel thickness has figured prominently in discussions of hominid origins for nearly a century, although little is known about its intra-taxon variation. It has been suggested that enamel thickness increases from first to third molars, perhaps due to varying functional demands or developmental constraints, but this has not been tested with appropriate statistical methods. We quantified enamel cap area (c), dentine area (b), and enamel-dentine junction length (e) in coronal planes of sections through the mesial and distal cusps in 57 permanent molars of Pan and 59 of Pongo, and calculated average (c/e) and relative enamel thickness (([c/e]/ radicalb) * 100). Posteriorly increasing or decreasing trends in each variable and average (AET) and relative enamel thickness (RET) were tested among molars in the same row. Differences between maxillary and mandibular analogues and between mesial and distal sections of the same tooth were also examined. In mesial sections of both genera, enamel cap area significantly increased posteriorly, except in Pan maxillary sections. In distal sections of maxillary teeth, trends of decreasing dentine area were significant in both taxa, possibly due to hypocone reduction. Significant increases in AET and RET posteriorly were found in all comparisons, except for AET in Pongo distal maxillary sections. Several significant differences were found between maxillary and mandibular analogues in both taxa. Relative to their mesial counterparts, distal sections showed increased enamel cap area and/or decreased dentine area, and thus increased AET and RET. This study indicates that when AET and RET are calculated from samples of mixed molars, variability is exaggerated due to the lumping of tooth types. To maximize taxonomic discrimination using enamel thickness, tooth type and section plane should be taken into account. Nonetheless, previous findings that African apes have relatively thinner enamel than Pongo is supported for certain molar positions.     

The dentition of the Indian Knoll skeletal population: odontometrics and cusp number.

Data on the permanent dentition of 153 individuals from the well known Indian Knoll skeletal population are presented. Mesiodistal and buccolingual measurements were taken with a Helios dial caliper. Cusp number of maxillary and mandibular molars are recorded. The Indian Knoll dentition is larger than many modern groups but smaller than Australoid or Mesolithic groups. With the exception of maxillary 12, males have larger teeth than females in both dimensions. The lower canine is the most dimorphic tooth. Through rank order correlation, an association was shown between the sexual dimorphism of the mesiodistal and buccolingual dimensions. Compared to modern groups, the Indian Knoll population displays a moderate degree of sexual dimorphism in tooth size. In general, the coefficients of variation were greater for the more distal teeth within morphological classes. Amounts of size variability did not differ significantly between the sexes; moreover, rank order correlations indicated that patterns of variability in both dimensions were similar for males and females. The predominant cusp number pattern for upper molars is 4-3-3 and for lowers 5-5(4)-5. No sex differences were shown for cusp occurrence or bilateral asymmetry in cusp number.