Sex determination in Miocene catarrhine primates

Canines of fossil hominoids and primitive catarrhines from several early, middle, and late Miocene sites were analyzed according to the shape indices described in Kelley (1995) and compared to those of males and females of extant great apes. In bivariate plots of the fossil canines utilizing the indices, 90% of the upper canines and 85% of the lower canines fell within or just outside the exclusively male or exclusively female territories delimited by the extant great apes. The remainder fell in the male-female overlap zones. Sex assignments based on these distributions were nearly 100% concordant with classifications according to canine height, suggesting a high degree of accuracy. There were various taxon-specific shifts in bivariate space among fossil genera, reflecting subtle differences in canine shape between taxa within the overall pattern of similarity to extant great apes as a whole. In many cases these shifts are matched by particular extant-ape species and subspecies, while other fossil taxa have no exact analogue for canine shape among the extant great apes. However, the pattern of spatial segregation of canines identified as either male or female at each of the sites largely mirrors that of males and females within the extant-ape sample, indicating that Miocene catarrhines shared with extant great apes a common pattern of shape differences between male and female canines, regardless of taxonspecific morphologies. These observations demonstrate that the canines of fossil catarrhines can be sexed with a high degree of confidence based solely on intrinsic features of shape. This will permit more reliable characterizations of morphological sexual dimorphism among fossil species. It is also argued that canine shape is a more reliable indicator of sex in fossil taxa than are canine/molar size ratios. © 1995 Wiley-Liss, Inc.     

SEX DETERMINATION OF THE CALIFORNIA SEA LION (ZALOPHUS CALIFORNIANUS CALIFORNIANUS) FROM CANINE TEETH

Size of canine teeth from California sea lion ( Zalophus californianus californianus ) carcasses is shown to be useful in determining the sex of animals which have missing genitalia or which are otherwise of unknown sex. A total of 267 canine teeth from carcasses of 68 males and 43 females were measured along five axes. Of root and crown measurements of upper and lower canines, males and females overlapped only in root thickness of upper canines. A multivariate ANOVA showed a significant difference in the size of canines between upper and lower canines, and between males and females. Stepwise discriminant analysis produced discriminant functions for upper and lower canines for determining sex of unknown-sexed California sea lions. A separate set of canine teeth from 39 male and 49 female California sea lions was correctly classified without prior knowledge of sex by visual inspection and by the two discriminant functions.     

Developmental Aspects of Sexual Dimorphism in Hominoid Canines

We examined the histology of canine teeth in extant hominoids and provided a comparative database on several aspects of canine development. The resultant data augment the known pattern of differences in aspects of tooth crown formation among great apes and more importantly, enable us to determine the underlying developmental mechanisms responsible for canine dimorphism in them. We sectioned and analyzed a large sample (n = 108) of reliably-sexed great ape mandibular canines according to standard histological techniques. Using information from long- and short-period incremental markings in teeth, we recorded measurements of daily secretion rates, periodicity and linear enamel thickness for specimens of Pan troglodytes, Gorilla gorilla, Pongo pygmaeus and Homo sapiens. Modal values of periodicities in males and females, respectively, are: Pan 7/7; Gorilla 9/10; Pongo 10/10; and Homo 8/8. Secretion rates increase from the inner to the outer region of the enamel cap and decrease from the cuspal towards the cervical margin of the canine crown in all great ape species. Female hominoids tend to possess significantly thicker enamel than their male counterparts, which is almost certainly related to the presence of faster daily secretion rates near the enamel-dentine junction, especially in Gorilla and Pongo. Taken together, these results indicate that sexual differences in canine development are most apparent in the earlier stages of canine crown formation, while interspecific differences are most apparent in the outer crown region. When combined with results on the rate and duration of canine crown formation, the results provide essential background work for larger projects aimed at understanding the developmental basis of canine dimorphism in extant and extinct large-bodied hominoids and eventually in early hominins.     

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.     

Sexual dimorphism in Laccopithecus robustus, a late miocene hominoid from China

Laccopithecus robustus is a siamang-sized fossil ape from the Miocene site of Lufeng, China. The species is known from a partial cranium, numerous mandibles, and scores of isolated teeth. This species shows striking dental similarities to Pliopithecus from the Miocene of Europe and a number of cranial similarities to extant gibbons. Laccopithecus differs from extant gibbons and resembles other fossil and extant apes in showing marked sexual dimorphism in the size and shape of the canines and anterior lower premolars. Evidence for sexual differences in either the size or shape of other teeth is less clear. There is some evidence for a sexual size dimorphism based on the variability of molar teeth.     

Morphological evidence for the biological role of caniniform teeth in combtooth blennies (Blenniidae, Teleostei)

Combtooth blennies have recurved, fang-like caniniform teeth at the rear end of a single row of incisiform teeth. The lengths and positions of these canines were measured in the lower jaws of males of 14 species of Mediterranean Blenniidae. In four species, lower jaw canines were measured in males and females, while in one species, the upper jaw canines of both sexes were also measured. Relative (to body length) canine length in males tends to be significantly greater (10–40%) than in females. There are significant interspecific differences in relative canine length, with smaller species tending to have relatively larger teeth. No significant correlation was obtained between canine length and importance of animal prey in the diet, nor with 'hole fit' of males, which may be related with the intensity of paternal care. We suggest that canines in combtooth blennies are predominately used for predator deterrence and agonistic interactions.     

An analysis of cercopithecoid odontometrics. I. The scaling of the maxillary dentition.

The relations between two tooth indices, post-canine area and incisor width in the upper jaw, and three variables, diet, body weight and body weight dimorphism, were examined separately for the males and females of 29 cercopithecoid species. Each species was assigned to one of three diet classes (folivore, frugivore, omnivore). Data on the other variable consisted of species means (log-transformed) obtained from published sources. The analytic techniques used were bivariate and multiple regression, the tooth indices being the dependent variables. All tooth indices scaled isometrically within diet classes, and all except female incisor width scaled with positive allometry across diet classes. In both sexes, the body weight adjusted mean incisor width of folivores was significantly smaller than that of either frugivores or omnivores. In the females, the body weight adjusted mean post-canine areas did not differ significantly across diet classes, while in the males the omnivores had a larger body weight adjusted mean post-canine area than either the folivores or frugivores. Female post-canine area was the only tooth index for which body weight dimorphism was a significant predictor. Extrapolations of these findings to other extant and to fossil primate species are discussed.     

Directional selection in the evolution of elongated upper canines in clouded leopards and sabre‐toothed cats

Extremely developed or specialized traits such as the elongated upper canines of extinct sabre‐toothed cats are often not analogous to those of any extant species, which limits our understanding of their evolutionary cause. However, an extant species may have undergone directional selection for a similar extreme phenotype. Among living felids, the clouded leopard, Neofelis nebulosa, has exceptionally long upper canines for its body size. We hypothesized that directional selection generated the elongated upper canines of clouded leopards in a manner similar to the process in extinct sabre‐toothed cats. To test this, we developed an approach that compared the effect of directional selection among lineages in a phylogeny using a simulation of trait evolution and approximate Bayesian computation. This approach was applied to analyse the evolution of upper canine length in the Felidae phylogeny. Our analyses consistently showed directional selection favouring longer upper canines in the clouded leopard lineage and a lineage leading to the sabre‐toothed cat with the longest upper canines, Smilodon. Most of our analyses detected an effect of directional selection for longer upper canines in the lineage leading to another sabre‐toothed cat, Homotherium, although this selection may have occurred exclusively in the primitive species. In all the analyses, the clouded leopard and Smilodon lineages showed comparable directional selection. This implies that clouded leopards share a selection advantage with sabre‐toothed cats in having elongated upper canines.     

Growth and Development in Wild Owl Monkeys (<Emphasis Type="Italic">Aotus azarai</Emphasis>) of Argentina

Life history predicts that in sexually dimorphic species in which males are the larger sex, males should reach sexual maturity later than females (or vice versa if females are the larger sex). The corresponding prediction that in sexually monomorphic species maturational rates will differ little between the sexes has rarely been tested. We report here sex differences in growth and development to adulthood for 70 female and 69 male wild owl monkeys (Aotus azarai). In addition, using evidence from natal dispersal and first reproduction (mean: 74 mo) for 7 individuals of known age, we assigned ages to categories: infant, 0–6 mo; juvenile, 6.1–24 mo; subadult, 24.1–48 mo; adult >48 mo. We compared von Bertalanffy growth curves and growth rates derived from linear piecewise regressions for juvenile and subadult females and males. Growth rates did not differ between the sexes, although juvenile females were slightly longer than males. Females reached maximum maxillary canine height at ca. 2 yr, about a year earlier than males, and females’ maxillary canines were shorter than males’. Thus apart from canine eruption and possibly crown–rump length, the development of Azara’s owl monkeys conforms to the prediction by life history that in monomorphic species the sexes should develop at similar paces.     

Metric variation and sexual dimorphism in the dentition of Ouranopithecus macedoniensis

The fossil sample attributed to the late Miocene hominoid taxon Ouranopithecus macedoniensis is characterized by a high degree of dental metric variation. As a result, some researchers support a multiple-species taxonomy for this sample. Other researchers do not think that the sample variation is too great to be accommodated within one species. This study examines variation and sexual dimorphism in mandibular canine and postcanine dental metrics of an Ouranopithecus sample. Bootstrapping (resampling with replacement) of extant hominoid dental metric data is performed to test the hypothesis that the coefficients of variation (CV) and the indices of sexual dimorphism (ISD) of the fossil sample are not significantly different from those of modern great apes. Variation and sexual dimorphism in Ouranopithecus M(1) dimensions were statistically different from those of all extant ape samples; however, most of the dental metrics of Ouranopithecus were neither more variable nor more sexually dimorphic than those of Gorilla and Pongo. Similarly high levels of mandibular molar variation are known to characterize other fossil hominoid species. The Ouranopithecus specimens are morphologically homogeneous and it is probable that all but one specimen included in this study are from a single population. It is unlikely that the sample includes specimens of two sympatric large-bodied hominoid species. For these reasons, a single-species hypothesis is not rejected for the Ouranopithecus macedoniensis material. Correlations between mandibular first molar tooth size dimorphism and body size dimorphism indicate that O. macedoniensis and other extinct hominoids were more sexually size dimorphic than any living great apes, which suggests that social behaviors and life history profiles of these species may have been different from those of living species.     

Canine Dimorphism and Interspecific Canine Form in Cebus

I investigated canine dimorphism and interspecific canine form in adult specimens from 4 capuchin species (Cebus albifrons, C. apella, C. capucinus, and C. olivaceus). I used various univariate and multivariate statistics, which are based on 6 variables, to test several hypotheses that are based upon the finding that canine dimorphism is strongly associated with intermale competition in platyrrhines (Kay et al., 1988), Greenfield (1992a), Plavcan and van Schaik (1992, 1994). Results from the indices of canine dimorphism and the unpaired t-tests corroborate the prediction that males of each species possess significantly larger canines than those of females. Large male canines are especially prominent in 2 variables, maxillary and mandibular canine height. Greene's t-test (1989) does not support the prediction that Cebus apella and C. olivaceus possess a larger degree of canine dimorphism relative to C. albifrons and C. capucinus. No interspecific differences in degree of canine dimorphism are indicated by this test. Results of the discriminant function analyses (DFA) do not find that Cebus apella and C. olivaceus possess different canine form relative to C. albifrons and C. capucinus as predicted. However, Cebus apella is differentiated from the untufted capuchins (C. albifrons, C. capucinus, and C. olivaceus) by the DFA. I suggest that intermale competition is the primary selective force underlying the observed morphological patterns; however, it does not explain all the variation associated with canine dimorphism in Cebus.     

Apes and Tricksters: The Evolution and Diversification of Humans’ Closest Relatives

The evolutionary history of humans comprises an important but small branch on the larger tree of ape evolution. Today’s hominoids—gibbons, orangutans, gorillas, chimpanzees, and humans—are a meager representation of the ape diversity that characterized the Old World from 23–5 million years ago. In this paper, I briefly review this evolutionary history focusing on features important for understanding modern ape and human origins. As the full complexity of ape evolution is beyond this review, I characterize major geographic, temporal, and phylogenetic groups using a few flagship taxa. Improving our knowledge of hominoid evolution both complicates and clarifies studies of human origins. On one hand, features thought to be unique to the human lineage find parallels in some fossil ape species, reducing their usefulness for identifying fossil humans. On the other hand, the Miocene record of fossil apes provides an important source for generating hypotheses about the ancestral human condition; this is particularly true given the dearth of fossils representing our closest living relatives: chimpanzees and gorillas.     

Hominoid dental variability and species number at the late Miocene site of Lufeng,China

The large hominoid sample from the late Miocene site of Lufeng, China, has been variously claimed to contain either one or two species, but very few metric data in support of either position have been published. We calculate coefficients of variation for the dental remains both for the two presumed species and for the pooled sample as a whole using the summary statistics published by Wu & Oxnard (Wu & Oxnard: American Journal of Primatology 5:303–344, 1983a, Nature 306:258–260, 1983b). These are compared to the same measures of single-sex and combined-sex samples of extant hominoids. We also present metric characterizations of male and female canines of extant great apes, with which we evaluate the gender composition of the Lufeng canine sample. In a two-species alternative, the two presumed species have measures of variability and canine representation that are more compatible with single-sex samples representing males and females, respectively. The pooled dental sample has measures of variability within the ranges of single species of extant great apes. We conclude there is a single large hominoid species represented at Lufeng that is highly sexually dimorphic. The phylogenetic relationships of this species are briefly considered. It is generally primitive in craniodental morhpology and is unlikely to be a member of the Sivapithecus-Pongo clade.     

Canine role in dental wear patterns: Macaca nemestrina

A study of variables and patterns in dental wear among 30 individuals in a colony of Macaca nemestrina shows that consideration of age and sex are crucial for understanding differential wear degrees on molar occlusal planes. With advanced age, this species of non-human primate undergoes obliteration of initial morphological characteristics through the gradual erosion of enamel. Wear gradients are differential from PM1-M3 in both sexes. It appears that there is a functional relationship between degrees of occlusal plane wear and the degree of wear on the canines, and that females show a greater degree of wear changes relative to males of equivalent age because of initial differences in canine length and robusticity due to sexual dimorphism. It appears that there is a direct relationship between occlusal wear plane changes and the degree of wear on the canines, with advanced differential wear showing up in individuals in whom years of maxillary canine honing, canine damage, and the normal wear of mastication has reduced dimensions of unworn permanent canines. Other considerations included in this study are the honing functions of the deciduous first mandibular molars and molar cusp height relative to canine function.     

Canine root development and morphology inMacaca nemestrina

Recently,Yoshikawa andDeguchi (1992) reported an unusually high frequency (40%) of two-rooted maxillary canines inMacaca fuscata females and a complete absence of this trait in males. In the present study, canine root development and morphology was examined using cephalographs taken on 50 male and 50 femaleMacaca nemestrina, and 20 male and 20 femalePapio cynocephalus for comparison with the Japanese macaque. The results showed no double-rooted canines present in either species in the upper or lower canines. This supports the general rule that, among primates, canines possess a single-root. It was further suggested that the two-rooted canines inM. fuscata may be the result of the founder effect, i.e. that the genes for this trait may have been carried by the initial populations when they arrived on the islands sometime during the middle to late Pleistocene.     

Canine teeth of the monkey,Callicebus moloch: Lack of sexual dimorphism

Unlike other primates, the South American titi monkey,Callicebus moloch, does not exhibit sex-differences in the size or shape of the canine teeth, or in the extent of loss or fracture from excessive use. Males and females have similar canines as well in each of six subspecies ofC. moloch. The lack of dimorphism is related to the low level of aggression in this species.     

Ramapithecus and Sivapithecus from China: Some implications for higher primate evolution

The pattern of overall dental dimensions in over 900 teeth of ramapithecines from Lufeng in China is examined using frequency distribution histograms and fitted normal curves, and compared with data for extant hominoids. A prior study has demonstrated unequivocally that at least two groups of animals must have existed at Lufeng [Wu and Oxnard, 1983; Oxnard, 1983a]. The present investigation confirms this finding in more detail. In addition it shows that one fossil group possesses smaller teeth with a lesser degree of sexual dimorphism and approximately equal numbers of adult males and females, and the other possesses larger teeth with a rather larger degree of sexual dimorphism and a female-male ratio that may have approximated from as low as 2:1 to as high as 4:1. Comparisons of patterns of difference along the tooth row demonstrate that both these forms differ from modern apes in their sexual dimorphism, the smaller form being more like humans than the larger, which is more like apes, especially orangutans. Comparisons of the areas of the canine teeth with each of the other functional segments of the tooth row again show that the smaller form is basically similar to modern humans and that the larger resembles extant great apes. Comparisons of other functional dental areas seem to relate to dietary and masticatory functions. Thus the cutting areas are large relative to the chewing areas in omnivorous humans, whereas in the essentially vegetarian great apes this ratio is smaller. The smaller fossil resembles the human condition and may have been somewhat omnivorous; the larger one more resembles the apes and may have been somewhat more vegetarian. However, these comparisons also show that the way in which the larger form resembles the apes is associated with special development of the canines, which is different from that in any modern ape. Comparisons show that the canines in the larger form project far beyond the normal line of tooth crowns. Finally, comparisons show that canine sexual dimorphism in height is marked in the larger form. Neither of these last two features is true of the smaller fossil. These findings have implications for our understanding of the evolution of early pongids and hominids, and for the evolution of primate sexual dimorphisms and dental mechanisms.     

Sexual dimorphism in Ivory-billed Woodcreepers (Xiphorhynchus flavigaster) in Mexico

We analyzed a sample of 173 specimens of different subspecies within the distribution of the Ivory-billed Woodcreeper (Xiphorhynchus flavigaster) in Mexico. Morphological variables were analyzed separately for males, females, juveniles, and adults. The results showed that males were larger in wing chord, tail length, body mass, and primary 8 length than females. Discriminant function analysis yielded correct classification as males or females in 95% of samples analyzed (92.3% of males and 100% of females). Additionally, we identified morphological variables which presented the highest correlation to obtain linear regression functions for estimating one or more missing variables in specimens. The discriminating function developed offers a means of determining the sex of individual Ivory-billed Woodcreepers, so this tool is valuable for ecological studies and population studies of this species.     

Crested gibbon (Hylobates [Nomascus]) identification using noninvasively obtained DNA

The development of captive breeding programs for the crested gibbons (Hylobates [Nomascus]) of Indochina is hindered by the difficulty of sorting individuals into their correct species and subspecies groups. We describe taxon-specific DNA sequence variation in a 252-base pair region of the mitochondrial cytochrome b gene, which can be used to identify individuals of the three taxa of crested gibbon commonly found in Western zoos. These molecular genetic markers can be amplified from plucked hair and will permit the identification of morphologically similar females and crested gibbons of either sex of unknown origin. Noninvasive genotyping of captive animals will facilitate the genetic management of these critically endangered primates. © 1994 Wiley-Liss, Inc.     

Sexual dimorphism in canine length of woolly spider monkeys (Brachyteles arachnoides,E. Geoffroy 1806)

We measured canine teeth from 28 woolly spider monkeys (Brachyteles arachnoides) to assess sexual dimorphism and population differences. The specimens are from the Brazilian states of Bahia, Minas Gerais, Espírito Santo, Rio de Janeiro, and São Paulo. We found strong sexual dimorphism in canine length for individuals belonging to populations south of 22°00 latitude but no sexual dimorphism in canine length from individuals of populations north of 21°00 latitude. Canine length did not vary among females of northern and southern populations. However, southern males had significantly longer canines than northern males. This geographical difference in canine morphology, together with the presence or absence of thumbs and published accounts of differences in genetics and social structure between northern and southern populations, suggests thatBrachyteles arachnoides may be composed of at least two subspecies, which appear to be separated by the rivers Grande and Paraiba do Sul and the Serra da Mantiqueira.