Ontogenetic approaches to sexual dimorphism in anthropoids

Studies of sexual dimorphism have traditionally focused on the static differences in size and shape between adult males and females. In this paper, I suggest that an investigation of the ontogenetic bases of sexual dimorphism can provide new insights and information unobtainable from studies concerned only with adult endpoints. While growth is often viewed as simply the developmental pathway utilized to attain final adult size and shape, we must recognize that it is the entire pattern of sex-differentiated growth, and not merely the adult endpoints, which is adaptive and the target of natural selection. The importance of an ontogenetic approach to the analysis of sexual dimorphism is also demonstrated by the fact that a given morphologicalresult (e.g., a certain degree of adult weight dimorphism) may be attained by very different developmentalprocesses, signalling selection for quite different factors. The need to analyze the ontogenetic bases of sexual dimorphism in size and shape has recently been recognized by Jarman, in his study of dimorphism in large terrestrial herbivores. Here I combine aspects of Jarman’s approach with those of allometry and heterochrony in an analysis of sexual dimorphism in selected anthropoid primates. It is demonstrated that although all dimorphic anthropoids appear to be characterized by somebimaturism, the degree varies significantly. Marked weight dimorphism in certain species is primarily produced by an increased differentiation of female and male growthrates, while in other species the primary change involves differences in thetime or duration of growth between the sexes. These variations are illustrated with anthropoid genera such asMiopithecus, Cercopithecus, Erythrocebus, Macaca, Papio, Pan, andGorilla. It is suggested that additional ontogenetic investigations of other anthropoids will help clarify some of the socioecological bases of this variation in the ways of attaining an adult dimorphic state. This will contribute to our understanding of the complex factors underlying and producing sexual dimorphism in primates and other mammals.     

Sexual dimorphism of the dental tissues in human permanent mandibular canines and third premolars

Methods of measuring tissue area from images of longitudinal thin tooth sections have been used to assess sexual dimorphism in the permanent dentition. The aim of this study was to demonstrate the extent of sexual dimorphism within the coronal tissue proportions of permanent mandibular canines and premolars, using area measurements of the enamel and dentine-pulp core. The sample consisted of embedded "half-tooth" sections from 45 individuals, all of known age-at-death and sex, collected from the St. Thomas' Anglican Church historic (1821-1874) cemetery site in Belleville, ON, Canada. The relative dentine-pulp area of the third premolars and canines displayed high levels of sexual dimorphism, as well as statistically significant mean differences between the sexes. The male canines and premolars have significantly more dentine than their female counterparts, as well as relatively more dentine with respect to overall crown size. The female canines and premolars have significantly more enamel relative to overall crown area than those of the males. These results suggest that relative area measures of crown tissues are more predictable measures of sexual dimorphism than absolute measures, and tissue proportions may remain constant despite intrasex variation in overall tooth crown size.     

Aluminum concentrations in human deciduous enamel and dentin related to dental caries

The aluminum (Al) concentrations in the enamel and dentin of 314 human deciduous teeth were determined in order to examine the relationship between Al and dental caries. The sample teeth were divided into three groups: the sound tooth group, carious tooth group and filled tooth group. The teeth of the carious tooth group were further classified into three groups depending on the stage of caries. The Al content was determined using graphite furnace atomic absorption spectrometry. In both the enamel and dentin, the Al concentrations were unaffected by sex, but did depend on tooth type. In enamel, the Al concentration was significantly higher in the sound tooth group (42.8 +/- 37.3 microg/g) than in the three carious groups (20.7 +/- 17.1-24.9 +/- 22.0 microg/g) and the filled tooth group (27.3 +/- 25.5 microg/g). As for dentin, the Al concentration was also significantly higher in the sound tooth group (36.2 +/- 35.1 microg/g) than in the three carious groups (15.1 +/- 13.3-24.5 +/- 23.4 microg/g) and the filled tooth group (17.2 +/- 20.6 microg/g). Even when analyzing incisors alone, the Al concentrations were significantly higher in the sound tooth group than in the other groups, for both enamel and dentin. Furthermore, the Al levels in carious enamel and dentin did not decrease with the advance of caries. These findings indicated that the deciduous teeth containing higher Al concentrations on average had less caries than the teeth with lower Al concentrations, and suggest that Al acts as a possible cariostatic agent by itself.     

Sexual dimorphism in crown units of mandibular deciduous and permanent molars in Australian Aborigines.

Sexual differences in the crown units of mandibular molars were investigated in Australian Aborigines. The first and second deciduous molars (dm1 and dm2), and first to third permanent molars (M1, M2 and M3) were measured on dental casts using a sliding caliper. Measurements of tooth crowns included overall mesiodistal and buccolingual diameters, as well as the mesiodistal and buccolingual diameters of the trigonid and talonid. Percentage dimorphism values were greater in the talonid dimensions than the trigonid, indicating that sex differences tend to be larger in the later-developing crown units. Sex differences in mesiodistal diameters increased from dm1 to M2 but decreased for M3, the tooth that showed the least dimorphism of all the molars. This result seems to be due to the marked variability in size of the M3 between individuals.     

Dental sexual dimorphism and morphology in african colobus monkeys as related to diet

We considered the relationship between dental sexual dimorphism and diet in 542 specimens of olive, red, and black-and-white colobus. Using univariate statistical techniques, we examined 41 measurements of the maxillary and mandibular dentitions. The results reveal two trends of dental sexual dimorphism in black-and-white colobus wherein (i) maleColobus guereza andC. angolensis are generally larger than females throughout the dentition and (ii)C. satanas and, to a lesser degree,C. polykomos exhibit reduced sexual differences in the canine base and females are slightly larger than males in noncanine dimensions. Females of the red colobus,Procolobus (Piliocolobus) badius, are slightly larger than males in most noncanine measurements but canine sex differences are more pronounced than those of black-and-white colobus.Procolobus (Procolobus) verus, the olive colobus, is characterized by some of the largest canine sex differences, yet the sexes do not differ much in noncanine mean values. When patterns of sexual dimorphism are considered in terms of specific ecology and behavior, it is possible to relate sex differences, in part, to known dietary differences. For example, overall dental morphology and the trend of sexual differences inC. satanas andC. polykomos seem to be associated with the consumption of a diet rich in seeds. The pattern of dental sexual dimorphism inC. badius may also be influenced by dietary factors in that their patrilineal social organization could restrict female access to certain foods thereby affecting rates of attrition and creating selection pressure for larger teeth. Relatively less is known of the ecology and social organization ofP. verus but their dental sexual dimorphism is possibly less related to dietary factors than is the case for red or black-and-white colobus.     

Heterochrony and sexual dimorphism in the skull of the Liberian chimpanzee (Pan troglodytes verus)

Allometric methods and theory derived from principles of relative growth provide new and powerful approaches to an understanding of the nature and development of sexual dimorphism among living primates. The Frankfurt collection of Liberian chimpanzee skulls and mandibles provides a large skeletal sample from a single natural population of wild shot animals, including individuals of all ages and both sexes, and allows investigation of allometric and heterochronic patterns of sexual dimorphism. Univariate, bivariate, and multivariate analyses are utilized in this study in order to ascertain the ontogenetic nature of male-female differences in the skull of the Liberian chimpanzee. The results of univariate and multivariate analyses indicate that, while overall levels of sexual dimorphism in the chimpanzee skull are small, the greatest differences are in dimensions of the viscerocranium, while neurocranial dimensions and orbital size tend to be less dimorphic. Bivariate regressions of 21 cranial variables against basicranial length document positive allometry in many facial and mandibular dimensions, and isometry or negative allometry for most neurocranial dimensions. The data confirm previous work in chimpanzees and other anthropoid primates suggesting that males and females are “ontogenetically scaled” in most cranial traits. That is, males and females share the same cranial growth trajectories, although ending up at different points. Both rate and time hypermorphosis are suggested as underlying causes of ontogenetic scaling in the Liberian chimpanzee.     

The differential expression of dental sexual dimorphism in subspecies ofColobus guereza

Data on dental sex differences in seven of the eight currently recognized subspecies of Colobus guerezareveals a range of expression of sexual dimorphism. Males of most subspecies are larger than females throughout the dentition and this is especially pronounced for the canines and P ₃ For C. g. guerezaand C. g. gallarum,however, sex differences in the canines and P ₃ are less pronounced and females are often slightly larger than males in noncanine dental measurements. C. guerezasspp. occupying comparable habitats express similarities in the degree of maxillary canine dimorphism. In addition, for those subspecies distributed above the equator, there is also a cline of decreasing maxillary canine dimorphism from west to east in a progressively more northern direction. This cline corresponds to the occupation of increasingly more arid habitats, and reduced dimorphism is the result of larger maxillary canine size in females. We propose that this pattern of sexual dimorphism is related to differences in the relative intensity of predation pressure, guereza social organization, and energetic considerations. That the mandibular canine does not exhibit a similar trend of sexual dimorphism suggests that larger maxillary canines in females may function as weapons.     

Gingival eruption sequences of permanent teeth in early hominids.

Gingival eruption of the permanent teeth of Australopithecus, Paranthropus, and early Homo, diagnosed from enamel scratches and facets, is similar save for two sequences: eruption of the canines relative to the premolars which may be sexually dimorphic; and agenesis of M3 with delayed eruption of M2, first seen in Homo at two million years. Gingival eruption sequences are similar also for early and modern Homo, except that in some individuals today M3, M2, M1 and I2 take longer to form and emerge through the gingiva as functioning teeth. Probably, from two million years to the present in the evolutionary history of Homo dental development slowed-down. More and more of ontogeny has been taken over for eruption.     

Sexual dimorphism in human skulls. A comparison of sexual dimorphism in different populations

Application and comparison of sex discriminant functions in different populations led to the conclusion that a certain combination and weighting of a few sex dimorphism variables (in this study we only used craniometric variables) can give a good discrimination between male and female individuals, independent of the racial group to which this function is applied. In our study, the sex-discriminatory power of five discriminant functions which were based on different ordination and selection procedures (e.g. professional knowledge, stepwise discriminant analysis, literature) of the cranial variables is compared. These discriminant functions were applied to three different data sets, the first being skull measurements from an Amsterdam series (Europids), the second skull measurements of a Zulu series (Negrids) and the third skull measurements of a Japan series (Mongolids). Our decision as to whether a function is a good or less good sex-discriminating function is determined by the Dt values (these values give an idea about the discriminatory value of the discriminant function when applied to a new test sample), the number of variables necessary to obtain this Dt and the location of the sectioning point (i.e. comparison between the estimation of the sectioning point and the ”real” sectioning point). These discriminant functions were compared withGiles Elliot's (1962, 1963) “race-independent” sex function.     

Unusually low sexual dimorphism of endocranial capacity in a Zulu cranial series

The mean cranial capacities of 50 male and 50 female Zulu crania were found to be 1373.3 +/- 107.4 ml for males and 1251.2 +/- 101.1 ml for females (means +/- SD). The male value resembles that of other Negro groups, while the female value is somewhat higher than the value for Negro crania as a whole. The index of sexual dimorphism is 8.9%, which is low when compared with those of other Negroid series and other populations. The possible causes for this form of a low sexual dimorphism are as follows: A negative secular trend, with the assumption that the Zulu crania were larger than those of the reference populations of African Negroids before the start of the secular trend change. This would seem to be the most likely possibility, with some supporting evidence for both parts of the explanation. An absence of secular trend, with a demographic sampling aberration, in which large females and small males of the population are sampled. This possibility cannot be totally excluded. An absence of secular trend, with a genetic difference in sexual dimorphism for cranial capacity between the Zulu and the reference populations. While this possibility cannot be excluded, it would be the least preferable explanation.     

Localization of 28 kDa calbindin in human odontoblasts

Summary The presence of 28 kDa calbindin in human odontoblasts was studied by use of specific antibodies raised against chick duodenal 28 kDa calbindin, in immunofluorescence, immuno-peroxidase, and electron-microscopic labelling experiments.The calbindin-like protein was detected mainly in the cytoplasm of odontoblast cell bodies, in their processes and occasionally in their nuclei. Correspondingly, at the ultrastructural level, immunoreactive material was associated with the cytosol, microfilaments and cilia. These findings suggest that human odontoblasts express a 28 kDa vitamin D-dependent calcium-binding protein, unlike those of rats and mice in which ameloblasts are the only cells immunoreactive for the protein.     

Statistical study of sexual dimorphism in the human fetal sciatic notch

Whether human fetal skeletal remains exhibit sexual dimorphism has been the subject of considerable debate. Most attention in this debate has focused on the greater sciatic notch of the ilium, since it is a gross morphological characteristic with known sex differences in the adult and is easily seen in fetal skeletal remains. Unfortunately, previous traditional morphometric analyses of the fetal sciatic notch have led to ambiguous results. The purpose of this study is to determine whether differences between the sexes can be discerned when modern morphometric techniques are applied to the fetal sciatic notch. Photographs of the ventral side of 133 fetal ilia of known age and sex from the Trotter Collection of Washington University were digitized, and the trace coordinates used for all subsequent analyses. The results of the analysis demonstrate that there is significant sexual dimorphism in the anterior to posterior location of the maximum depth of the sciatic notch, but that the depth of the notch itself is not dimorphic. While there is significant sexual dimorphism in the shape of the sciatic notch, the amount of overlap between males and females is too great for the sciatic notch to be used as a reliable indicator of sex. © 1995 Wiley-Liss, Inc.     

Attempts to label matrix synthesis of human root cementum in vitro

The present study describes the dynamic process of both acellular extrinsic (AEFC) and acellular/cellular intrinsic fiber cementum (AIFC/CIFC) matrix production on growing human teeth. Selected erupting maxillary and mandibular premolars with roots grown to about 70%–95% of their final length were placed in organ culture immediately following extraction. Twelve teeth for short-time labeling were pulse-incubated for 15 min in medium containing ³H-proline and chased for various times in order to follow the migration and secretion of the tracer. Eight teeth for long-time incubation were labeled continuously for 5 h before being chased for 1–8 days in order to label cementum matrix accumulation. After decalcification in ethylene diaminetetraacetic acid (EDTA), their roots were subdivided into about 20 slices each. Epon-embedded sections were prepared for light- and electron-microsopic as well as autoradiographic examination. During CIFC-formation, cementoblasts revealed high intracytoplasmic silver grain concentrations within the first hour after ³H-proline administration. The release of the tracer occurred between 60 to 120 min after administration. After 2 h, cementoblasts and the cementum matrix appeared to be labeled about equally. After 5 h, most of the labeled proteins appeared to be localized in the cementoid. Silver grains increased in number over the cementum matrix from 5–24 h. Very high intracellular grain concentrations within very large cementoblasts corresponded to regions of rapid cementum formation. Tracer-halos around entrapped cells lend support to a multipolar mode of matrix production during CIFC-initiation. The fate of the tracer during the development of early AEFC-matrix was less clear. However, fibroblasts revealed dense intracytoplasmic grain accumulations within the first hour after ³H-proline administration. Thereafter, the tracer localization was vague. This indistinct grain localization reflected the particular mode of AEFC-matrix production characterized by addition of new fibril segments to pre-existing fibers of a collagenous fringe.     

Biometrical studies upon hominoid teeth: the coefficient of variation, sexual dimorphism and questions of phylogenetic relationship

Sexual dimorphism as a function of variation in hominoid tooth metrics has been investigated for four groups of taxa: Recent great apes (two subfamilies), Dryopiths (one subfamily), Ramapiths (one subfamily) and hominids (one family). Gorilla, and to a lesser extent Pan, appear characterized by very high levels of sexual dimorphism and meet several criteria for statistical outliers. Recent great apes are the only group exhibiting consistently high levels of sexual dimorphism. Ramapiths are the only group characterized by low levels of sexual dimorphism and their relative canine length is most similar to Dryopiths. Both Dryopiths and hominids contain taxa with low and intermediate levels of sexual dimorphism. The Gingerich and Shoeninger hypothesis relating coefficients of variation to occlusal complexity is supported. Non-parametric statistics suggest that homogeneity of coefficient of variation profiles over most of the tooth row is characteristic of only the Dryopiths and a composite data set composed of the Dryopith plus Ramapith tooth measurements. Oxnard's model for the multifactorial basis of multiple sexual dimorphisms is also supported. The Dryopith and hominid patterns of sexual dimorphism are similar, an observation that suggests phylogenetic relationship. At the taxonomic level of subfamily or family, sexual dimorphism is a character of cladistic usefulness and possible phylogenetic valence. Assuming that breeding system and sexual dimorphism are functional correlates as many workers suggest, then Ramapithecus sp. China, Sivapithecus indicus and possibly Australopithecus boisei are good candidates for having possessed monogamous breeding/social structures. All Dryopith taxa, S. sivalensis, Sivapithecus sp. China, A. afarensis, Homo habilis and H. erectus emerge as the best candidates for having possessed a polygynous breeding/social structure. No biometrical affinities of Ramapiths with hominids can be demonstrated and some phylogenetic relationship with Dryopiths is suggested. Kay's interpretation of Ramapith sexual dimorphism and taxonomic affinity is not supported. The lack of control over temporal and geographic range variation is discussed and the loose association of these variables with differences in tooth morphology is noted. The high heritability of tooth size also suggests that assignment of "high" or "low" index values to extinct taxa as a measure that describes evolving clades at discrete points in evolutionary time is appropriate.(ABSTRACT TRUNCATED AT 400 WORDS)     

Initial formation of cellular intrinsic fiber cementum in developing human teeth

Summary The present study describes the formative process of the initiation of cellular intrinsic fiber cementum (CIFC) in still growing human teeth. From 29 premolars and molars with incomplete roots developed to 60–90% of their final length, 8 premolars (with roots formed to three quarters of their final length) were selected for electron-microscopic investigation. All teeth were clinically intact and prefixed in Karnovsky's fixative immediately after extraction. Most of them were decalcified in ethylene diaminetetraacetic acid (EDTA), and the apical part of the roots was divided axially into mesial and distal portions that were subdivided in about 5 slices each. Following osmication and embedding in Epon, these blocks were cut for light- and electron-microscopic examination. In addition, 5 teeth with incomplete roots were freed from organic material and processed for scanning electron microscopy. It was found that CIFC-initiation commenced very close to the advancing root edge and resulted in a rapid cementum thickening. Thereafter, appositional growth continued on the already established cementum surface. Large, basophilic and rough endoplasmic reticulum-rich cementoblasts, some of which became cementocytes, were responsible for both fast and slow CIFC-formation. The CIFC-matrix was free of Sharpey's fibers and composed of more or less organized intrinsic collagen fibrils, in part fibril bundles, that ran roughly parallel to the root surface. Initially, the cementum fibrils intermingled with those of the dentinal collagen fibrils, which were not yet mineralized. This boundary subsequently underwent calcification. The development of collagen fibril bundles and their extracellular arrangement were associated with cytoplasmic processes probably involved in fibril formation and fibril assembly. Many cementoblasts contained intracytoplasmic, membrane-bounded collagen fibrils, which probably were related to fibril formation rather than degradation.     

Non-occlusal dental microwear variability in a sample of Middle and Late Pleistocene human populations from Europe and the Near East

Non-occlusal, buccal tooth microwear variability has been studied in 68 fossil humans from Europe and the Near East. The microwear patterns observed suggest that a major shift in human dietary habits and food processing techniques might have taken place in the transition from the Middle to the Late Pleistocene populations. Differences in microwear density, average length, and orientation of striations indicate that Middle Pleistocene humans had more abrasive dietary habits than Late Pleistocene populations. Both dietary and cultural factors might be responsible for the differences observed. In addition, the Middle Paleolithic Neanderthal specimens studied show a highly heterogeneous pattern of microwear when compared to the other samples considered, which is inconsistent with a hypothesis of all Neanderthals having a strictly carnivorous diet. The high density of striations observed in the buccal surfaces of several Neanderthal teeth might be indicative of the inclusion of plant foods in their diet. The buccal microwear variability observed in the Neanderthals is compatible with an overall exploitation of both plant and meat foods on the basis of food availability. A preliminary analysis of the relationship between buccal microwear density and climatic conditions prevailing in Europe during the Late Pleistocene has been attempted. Cold climatic conditions, as indicated by oxygen isotope stage data, seem to be responsible for higher densities of microwear features, whereas warmer periods could correspond to a reduced pattern of scratch density. Such a relationship would be indicative of less abrasive dietary habits, perhaps more meat dependent, during warmer periods.     

Further evidence on relative dental maturation and somatic developmental rate in hominoids.

New data on hominoid dental development are presented. Individual bivariate pairings of all mandibular teeth were made for African apes and humans. Data were analyzed with a full linear regression model. No statistically significant differences were found among apes, although a consistent pattern of earlier incisal development was observed in Pan relative to Gorilla. This is concordant with an earlier fusion of the premaxillary:maxillary suture in Pan. Only one tooth pair differed significantly by sex among apes. Two biologically distinct human samples (Libben and Hamann-Todd), although assessed differently (extraction and radiography) yielded virtually identical results. Humans differ from apes only by earlier relative calcification of their anterior teeth. This can be viewed as a consequence of reduced facial prognathism and a shift in hominid canine function.