Canine size and shape in male anthropoid primates

While studies of canine dimorphism in primates are common, only a few have examined canine tooth size independently within each sex. Recently, Greenfield and Washburn (Am. J. Phys. Anthropol. 84:17–34, 1991) proposed that there are two types of male canines which reflect different allometric scaling patterns of canine crown height against canine occlusal dimensions. They also suggest that proportional canine shape, measured as canine crown height (or projection) relative to the occlusal dimensions, provides an estimate of the canine's function as a weapon, though they provide no test of this hypothesis. This analysis critically examines the claim that there are two types of male canines among anthropoids. It then tests the hypothesis that relative male canine size (measured against body weight) and proportional canine shape are related to estimates of intermale competition, diet, and substrate (used as a surrogate measure of predation pressure). While there is strong taxonomic variation in canine size and shape among male anthropoids, no evidence is found for two discrete canine types. Rather, within families and subfamilies, canine dimensions scale isometrically against body weight and against each other, with a continuum of canine shapes among different taxa. While variation in male canine size is associated with intermale competition and substrate, even when taxonomic variation is controlled, variation in proportional canine shape is not. Neither canine size nor shape are generally associated with variation in diet. © 1993 Wiley-Liss, Inc.     

Canine Length in Wild Male Baboons: Maturation,Aging and Social Dominance Rank

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

Sexual dimorphism of tooth size in anthropoids

We have examined the size of the canine and postcanine teeth of cebid and catarrhine primates in relation to each other, to jaw size and to body weight. We have found that the canine size of males is large enough to be limited by jaw shape and size. A large contribution of P4 to the postcanine row is associated with smaller canines in males. Neither factor seems to limit canine size in females. The females of a small number of species possess enlarged canines. Much of the variation of the postcanine row can be described by the ratio of the (nominal) crown areas of M1 to M3. This ratio is monomorphic which conforms with the general lack of dietary dimorphism in primates. A brief discussion of the evolution of canine size is offered with a new suggestion to account for canine reduction in male hominids.     

Intrasexual selection and phylogenetic constraints in the evolution of sexual canine dimorphism in strepsirhine primates

The goals of this study were to analyze the origin and function of sex differences in the size of canine teeth among Malagasy lemurs and other strepsirhine primates. These analyses allowed me to illuminate interactions between different mechanisms of sexual selection and to elucidate constraints on this sexually-selected trait. In contrast to central predictions of sexual selection theory, polygynous lemurs lack both sexual dimorphism in body size and male social dominance, but the degree of sexual dimorphism in the size of their canines is not known. A comparison of male and female canine size in 31 species of lemurs and lorises revealed significant male-biased canine dimorphism in only 6 of 13 polygynous lemur species. This result is in contrast to predictions of a hypothesis that would explain the lack of size dimorphism in lemurs as a result of high viability costs because canine teeth presumably have low maintenance costs and because they are used as weapons in male-male combat. Moreover, because females had significantly larger maxillary canines than males in only one lemur species, female dominance is not generally based on female physical superiority and selective forces favoring female dominance do not constrain sexual canine dimorphism in the sense of a pleiotropic effect. Contrary to predictions of sexual selection theory, species differences in canine dimorphism across strepsirhines were neither associated with differences in mating system, nor with the potential frequency of aggression. Variation in canine dimorphism was also unrelated to differences in body size, but there were significant differences among families, pointing to strong phylogenetic constraints. This study demonstrated that polygynous lemurs are at most subject to weak intrasexual selection on dental traits used in male combat and that traits thought to be under intense sexual selection are strongly influenced by phylogenetic factors.     

Canine tooth size and fitness in male mandrills (Mandrillus sphinx)

Sexual selection theory explains the evolution of exaggerated male morphologies and weaponry, but the fitness consequences of developmental and age-related changes in these features remain poorly understood. This long-term study of mandrill monkeys (Mandrillus sphinx) demonstrates how age-related changes in canine tooth weaponry and adult canine size correlate closely with male lifetime reproductive success. Combining long-term demographic and morphometric data reveals that male fitness covaries simply and directly with canine ontogeny, adult maximum size, and wear. However, fitness is largely independent of other somatometrics. Male mandrills sire offspring almost exclusively when their canines exceed approximately 30 mm, or two-thirds of average adult value (45 mm). Moreover, sires have larger canines than nonsires. The tooth diminishes through wear as animals age, corresponding with, and perhaps influencing, reproductive senescence. These factors combine to constrain male reproductive opportunities to a brief timespan, defined by the period of maximum canine length. Sexually-selected weaponry, especially when it is nonrenewable like the primate canine tooth, is intimately tied to the male life course. Our analyses of this extremely dimorphic species indicate that sexual selection is closely intertwined with growth, development, and aging, pointing to new directions for sexual selection theory. Moreover, the primate canine tooth has potential as a simple mammalian system for testing genetically-based models of aging. Finally, the tooth may record details of life histories in fossil primates, especially when sexual selection has played a role in the evolution of dimorphism.     

Phylogenetic analyses of dimorphism in primates: evidence for stronger selection on canine size than on body size

Phylogenetic comparative methods were used to analyze the consequences of sexual selection on canine size and canine size dimorphism in primates. Our analyses of previously published body mass and canine size data revealed that the degree of sexual selection is correlated with canine size dimorphism, as well as with canine size in both sexes, in haplorhine but not in strepsirrhine primates. Consistent with these results, male and female canine size was found to be highly correlated in all primates. Since canine dimorphism and canine size in both sexes in haplorhines were found to be not only related to mating system but also to body size and body size dimorphism (characters which are also subject to or the result of sexual selection), it was not apparent whether the degree of canine dimorphism is the result of sexual selection on canine size itself, or whether canine dimorphism is instead a consequence of selection on body size, or vice versa. To distinguish among these possibilities, we conducted matched-pairs analyses on canine size after correcting for the effects of body size. These tests revealed significant effects of sexual selection on relative canine size, indicating that canine size is more important in haplorhine male-male competition than body size. Further analyses showed, however, that it was not possible to detect any evolutionary lag between canine size and body size, or between canine size dimorphism and body size dimorphism. Additional support for the notion of special selection on canine size consisted of allometric relationships in haplorhines between canine size and canine size dimorphism in males, as well as between canine size dimorphism and body size dimorphism. In conclusion, these analyses revealed that the effects of sexual selection on canine size are stronger than those on body size, perhaps indicating that canines are more important than body size in haplorhine male-male competition.     

Canine tooth size variability in primates

I present an analysis of canine tooth size variability in male and female primates. The coefficient of variation (CV = SD X 100/mean) as an index of canine size variability proved to be dependent on mean canine size in males and, to a lower extent, in females. Therefore, variability tends to increase with increasing values of mean canine size. Using residuals from the regression of log SD on log mean canine size in male and female primates, I analysed the contribution of diet, habitat and mating system to canine size variability. Habitat and mating system are known to influence to a certain extent the degree of sexual dimorphism in canine size. Given the well-known relationship between sexual dimorphism and phenotypic variability, it was suggested that these factors might influence variability in canine size. Everything else being equal, males of polygynous species are characterized by more variable canine sizes than males of monogamous species. Habitat and diet did not contribute to the level of variability observed in either males or females. It is proposed that a high level of variability in canine size may be related to the likelihood that enlarged canines evolved as a result of male-male competition for mates in polygynous species.     

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.     

Sexual Size Dimorphism,Canine Dimorphism,and Male-Male Competition in Primates

Sexual size dimorphism is generally associated with sexual selection via agonistic male competition in nonhuman primates. These primate models play an important role in understanding the origins and evolution of human behavior. Human size dimorphism is often hypothesized to be associated with high rates of male violence and polygyny. This raises the question of whether human dimorphism and patterns of male violence are inherited from a common ancestor with chimpanzees or are uniquely derived. Here I review patterns of, and causal models for, dimorphism in humans and other primates. While dimorphism in primates is associated with agonistic male mate competition, a variety of factors can affect male and female size, and thereby dimorphism. The causes of human sexual size dimorphism are uncertain, and could involve several non-mutually-exclusive mechanisms, such as mate competition, resource competition, intergroup violence, and female choice. A phylogenetic reconstruction of the evolution of dimorphism, including fossil hominins, indicates that the modern human condition is derived. This suggests that at least some behavioral similarities with Pan associated with dimorphism may have arisen independently, and not directly from a common ancestor.     

Static intraspecific allometry of the dentition in Otoletnur crassicaudatus

Adult static intraspecific allometry of tooth size was evaluated in a sample of 66 Otolemur crassicaudatus (34 male, 32 female). Tooth areas were calculated from mesiodistal and buccolingual measurements of canines and postcanine teeth of both arcades and were scaled to four viscerocranial measurements: bimaxillary width; maxillo-alveolar length; mandibular length and bigonial width. Individual tooth crown areas were also scaled to total skull length, body length and body weight. From the log-transformed analyses it is concluded that postcanine tooth size was unrelated to body length or weight, and poorly correlated to skull length or jaw size. Although viscerocranial size appears to be independent of body size, these measures are well correlated to skull length. It is shown that the longer the skull, the shorter and narrower the maxilla, and the longer and broader the mandible. Canines are shown to scale negatively allometric to skull length, hence, large animals will have relatively small canines.     

New faces of Aegyptopithecus from the Oligocene of Egypt

Three recently discovered faces of Aegyptopithecus zeuxis from the Oligocene Jebel Qatrani Formation of Egypt provide new information about the shape and variation of the facial cranium, the earliest preserved for a presumed forerunner of apes and humans. Although varying considerably in details of shape and proportion, the new finds and a skull found in 1966 all appear to be of males, a conclusion based in part on the development of temporal and sagittal crests and on the large size of upper canines or their sockets (female canines are much smaller). The snouts of the three new faces all are shorter and broader than that of the earlier found skull as reconstructed. As in most later species of Anthropoidea, variation between these specimens is high.Aegyptopithecus helps define the nature of the oldest Anthropoidea and generally most resembles later-occurring apes. Many features, both derived and shared primitive, link Aegyptopithecus, the large Miocene great apes of the Proconsul group, and modern great apes. That these shared features and proportions are not direct allometric consequences of body size is indicated by Aegyptopithecus' resemblance to the large apes and its many distinctions from similar-sized Hylobates.In Aegyptopithecus brain volume scales smaller than in later catarrhines relative to facial size, the ectotympanic tube is less developed and the premaxilla is more primitive than in later higher primates. In closure of orbits and conformation of forehead, face and dentition, Aegyptopithecus closely resembles higher primates and not prosimians. Taken together, its overall cranial and dental anatomy constitutes one of the most important connecting links in primate evolutionary history.     

Ontogeny of canine dimorphism in extant hominoids.

Many behavioral and ecological factors influence the degree of expression of canine dimorphism for different reasons. Regardless of its socioecological importance, we know virtually nothing about the processes responsible for the development of canine dimorphism. Our aim here is to describe the developmental process(es) regulating canine dimorphism in extant hominoids, using histological markers of tooth growth. Teeth preserve a permanent record of their ontogeny in the form of short- and long-period incremental markings in both enamel and dentine. We selected 52 histological sections of sexed hominoid canine teeth from a total sample of 115, from which we calculated the time and rate of cuspal enamel formation and the rate at which ameloblasts differentiate along the future enamel-dentine junction (EDJ) to the end of crown formation. Thus, we were able to reconstruct longitudinal growth curves for height attainment in male and female hominoid canines. Male hominoids consistently take longer to form canine crowns than do females (although not significantly so for our sample of Homo). Male orangutans and gorillas occasionally take up to twice as long as females to complete enamel formation. The mean ranges of female canine crown formation times are similar in Pan, Gorilla, and Pongo. Interspecific differences between female Pan canine crown heights and those of Gorilla and Pongo, which are taller, result from differences in rates of growth. Differences in canine crown heights between male Pan and the taller, more dimorphic male Gorilla and Pongo canines result both from differences in total time taken to form enamel and from faster rates of growth in Gorilla and Pongo. Although modern human canines do not emerge as significantly dimorphic in this study, it is well-known that sexual dimorphism in canine crown height exists. Larger samples of sexed modern human canines are therefore needed to identify clearly what underlies this.     

Evaluating the “dual selection” hypothesis of canine reduction

A recently proposed model for canine reduction in hominid evolution (the “dual selection” model) suggests that canine reduction occurs as a result for incorporation of the canines into a functional incisal field. Among the evidence used to support this model are patterns of wear and occlusion of the canine teeth, particularly in female anthropoid primates. We examined wear and occlusal patterns of the canine teeth of 311 male and female anthropoid primates. We find no evidence that the canines are typically occluded tip-to-tip, or that they show wear patterns indicating a “gripping and pulling” function during food ingestion and processing. Furthermore, we do not find compelling evidence that the development of the mesial cristid is associated with canine reduction. While we agree that the mechanisms of selective pressures underlying canine reduction need to be investigated, the “dual selection” hypothesis is unsupported by comparative data. © 1996 Wiley-Liss, Inc.     

Morphological Variation in Populations of <Emphasis Type="Italic">Eulemur albocollaris</Emphasis> and <Emphasis Type="Italic">E. fulvus rufus</Emphasis>

Sexual dimorphism in body size and canine weaponry is commonly associated with high levels of male-male competition. When group living species do not rely heavily on male-male competition for access to females, sperm competition may represent a viable alternative strategy. Unlike most haplorhine primates, lemurs are typically monomorphic in body weight and canine height. We assessed variability of body mass dimorphism and canine size dimorphism in brown lemurs using morphometric data from 3 populations in southeastern Madagascar: Eulemur fulvus rufus, E. albocollaris, and hybrids of the species. We found significant male-biased canine dimorphism in E. albocollaris in conjunction with body-size monomorphism. We observed similar patterns in the hybrids, but E. fulvus rufus exhibited significant female-biased size dimorphism and canine monomorphism. Testes volume was relatively high across study populations. Thus, sperm competition appears to be strong in brown lemurs. E. albocollaris males combine sperm competition with large canines, but not higher body mass, indicating a difference in sexual strategy from most lemurs. Patterns of body mass and canine size dimorphism are not uniform across brown lemur populations, indicating that future work on these populations can explicitly test models that predict relationships between size dimorphism and various types of competition.     

Estimating canine tooth crown height in early Australopithecus

Canine tooth size reduction and the associated reduction in canine dimorphism is a basal hominin character that also provides important evidence for models of behavioral evolution. Two specimens of Australopithecus anamensis (KNM-KP 29287 and KNM-KP 29283) that do not preserve the canine crown, but do preserve the root or alveolus, appear to suggest that canine size variation and canine dimorphism in this species may have been greater than in other hominins. We evaluate canine root and crown dimensions in a series of extant hominoids, and estimate canine crown height in Australopithecus afarensis and A. anamensis. Our results demonstrate that it is possible to generate estimates of canine crown height from basal canine crown and root dimensions with a moderate degree of accuracy. Estimates of maxillary canine crown size for A. anamensis are slightly larger than those of A. afarensis, and are approximately the same size as canines of modern female chimpanzees. Estimated mandibular canine crown height is very similar in the two species. Variation within the A. anamensis sample of estimated canine crown heights is similar to that of modern humans, suggesting a low degree of sexual dimorphism. Inclusion of estimates for KNM-KP 29287 and KNM-KP 29283 does not substantially increase either the estimate of overall canine size or variation for A. anamensis.     

Feeding ecology and morphology of the upper canines in bears (carnivora: Ursidae)

The morphology and mechanical strength of the upper canines in all eight extant species of ursids is analyzed, and the findings are discussed in relation to feeding ecology. Ursids have proportionally smaller canines than other large carnivores with a specialized feeding ecology, such as large felids, and the upper canine morphology is both canid‐like and felid‐like. The giant panda is the most divergent species, and its short, blunt, and cone‐like canines appear well adapted for tearing into bamboo. The almost equally herbivorous spectacled bear has a less derived canine morphology. The large canines of the sun bear are divergent from other ursine ursids, and may be an adaptation for tearing open tree trunks in search of insects. Discriminant Analysis is successful in separating ursid species on the basis of canine morphology, but the canines of ursine ursids, and also of the spectacled bear, show greater resemblance among the species than the marked differences in feeding ecology would suggest. This could be in part due to a short evolutionary history, and in part due to canines not having been subjected to much evolutionary selection as has been the case among other large carnivores, such as large felids. Ursids are probably evolutionarily and ecologically successful due to physical size and strength rather than a derived craniodental anatomy. J. Morphol., 2008. © 2008 Wiley‐Liss, Inc.     

Society, demography and genetic structure in the spotted hyena

Spotted hyenas (Crocuta crocuta) are large mammalian carnivores, but their societies, called 'clans', resemble those of such cercopithecine primates as baboons and macaques with respect to their size, hierarchical structure, and frequency of social interaction among both kin and unrelated group-mates. However, in contrast to cercopithecine primates, spotted hyenas regularly hunt antelope and compete with group-mates for access to kills, which are extremely rich food sources, but also rare and ephemeral. This unique occurrence of baboon-like sociality among top-level predators has favoured the evolution of many unusual traits in this species. We briefly review the relevant socio-ecology of spotted hyenas, document great demographic variation but little variation in social structure across the species' range, and describe the long-term fitness consequences of rank-related variation in resource access among clan-mates. We then summarize patterns of genetic relatedness within and between clans, including some from a population that had recently gone through a population bottleneck, and consider the roles of sexually dimorphic dispersal and female mate choice in the generation of these patterns. Finally, we apply social network theory under varying regimes of resource availability to analyse the effects of kinship on the stability of social relationships among members of one large hyena clan in Kenya. Although social bonds among both kin and non-kin are weakest when resource competition is most intense, hyenas sustain strong social relationships with kin year-round, despite constraints imposed by resource limitation. Our analyses suggest that selection might act on both individuals and matrilineal kin groups within clans containing multiple matrilines.     

Developmental processes and canine dimorphism in primate evolution

Understanding the evolutionary history of canine sexual dimorphism is important for interpreting the developmental biology, socioecology and phylogenetic position of primates. All current evidence for extant primates indicates that canine dimorphism is achieved through bimaturism rather than via differences in rates of crown formation time. Using incremental growth lines, we charted the ontogeny of canine formation within species of Eocene Cantius, the earliest known canine-dimorphic primate, to test whether canine dimorphism via bimaturism was developmentally canalized early in primate evolution. Our results show that canine dimorphism in Cantius is achieved primarily through different rates of crown formation in males and females, not bimaturism. This is the first demonstration of rate differences resulting in canine dimorphism in any primate and therefore suggests that canine dimorphism is not developmentally homologous across Primates. The most likely interpretation is that canine dimorphism has been selected for at least twice during the course of primate evolution. The power of this approach is its ability to identify underlying developmental processes behind patterns of morphological similarity, even in long-extinct primate species.     

Sexual dimorphism in postcranial skeletal shape suggests male-biased specialization for physical competition in anthropoid primates

Sexual dimorphism often arises as a response to selection on traits that improve a male's ability to physically compete for access to mates. In primates, sexual dimorphism in body mass and canine size is more common in species with intense male–male competition. However, in addition to these traits, other musculoskeletal adaptations may improve male fighting performance. Postcranial traits that increase strength, agility, and maneuverability may also be under selection. To test the hypothesis that males, as compared to females, are more specialized for physical competition in their postcranial anatomy, we compared sex-specific skeletal shape using a set of functional indices predicted to improve fighting performance. Across species, we found significant sexual dimorphism in a subset of these indices, indicating the presence of skeletal shape sexual dimorphism in our sample of anthropoid primates. Mean skeletal shape sexual dimorphism was positively correlated with sexual dimorphism in body size, an indicator of the intensity of male–male competition, even when controlling for both body mass and phylogenetic relatedness. These results suggest that selection on male fighting ability has played a role in the evolution of postcranial sexual dimorphism in primates.