Canine size, shape, and bending strength in primates and carnivores

Anthropoid primates are well known for their highly sexually dimorphic canine teeth, with males possessing canines that are up to 400% taller than those of females. Primate canine dimorphism has been extensively documented, with a consensus that large male primate canines serve as weapons for intrasexual competition, and some evidence that large female canines in some species may likewise function as weapons. However, apart from speculation that very tall male canines may be relatively weak and that seed predators have strong canines, the functional significance of primate canine shape has not been explored. Because carnivore canine shape and size are associated with killing style, this group provides a useful comparative baseline for primates. We evaluate primate maxillary canine tooth size, shape and relative bending strength against body size, skull size, and behavioral and demographic measures of male competition and sexual selection, and compare them to those of carnivores. We demonstrate that, relative to skull length and body mass, primate male canines are on average as large as or larger than those of similar sized carnivores. The range of primate female canine sizes embraces that of carnivores. Male and female primate canines are generally as strong as or stronger than those of carnivores. Although we find that seed-eating primates have relatively strong canines, we find no clear relationship between male primate canine strength and demographic or behavioral estimates of male competition or sexual selection, in spite of a strong relationship between these measures and canine crown height. This suggests either that most primate canines are selected to be very strong regardless of variation in behavior, or that primate canine shape is inherently strong enough to accommodate changes in crown height without compromising canine function.     

Canine tip wear in male and female anthropoids

One component of the “dual selection hypothesis” (Greenfield [1992a] Year. Phys. Anthropol. 35:153–185) is that the tips of female canines are commonly blunted and more frequently so than those of conspecific males. Data derived from two randomly selected age-graded samples of Macaca fascicularis (n = 70) and Colobus badius (n = 59) show that at least 80% of the females exhibit tip blunting on one or both canines and that frequencies of blunting are far greater than those of conspecific males in both jaws. Sexual dimorphism in mandibular canine morphology and wear and other recently critiqued aspects of the “dual selection hypothesis” (Plavcan and Kelley [1996] Am. J. Phys. Anthropol. 99:379–387.) are also discussed. Am J Phys Anthropol 107:87–97. © 1998 Wiley-Liss, Inc.     

Intrasexual competition and canine dimorphism in anthropoid primates.

A number of factors, including sexual selection, body weight, body-weight dimorphism, predation, diet, and phylogenetic inertia have been proposed as influences on the evolution of canine dimorphism in anthropoid primates. Although these factors are not mutually exclusive, opinions vary as to which is the most important. The role of sexual selection has been questioned because mating system, which should reflect its strength, poorly predicts variation in canine dimorphism, particularly among polygynous species. Kay et al. (1988) demonstrate that a more refined estimate of intermale competition explains a large proportion of the variation in canine dimorphism in platyrrhine primates. We expand their analysis, developing a more generalized measure of intermale competition based on the frequency and intensity of male-male agonism. We examine the relative influences of predation (inferred by substrate use), female body weight, body-weight dimorphism, diet, and sexual selection on the evolution of anthropoid canine dimorphism. Intermale competition is very strongly associated with canine dimorphism. Predation also has a marked effect on canine dimorphism, in that savanna-dwelling species consistently show greater canine dimorphism than other species, all other factors being held equal. Body-weight dimorphism is also strongly associated with canine dimorphism, though apparently through a common selective basis, rather than through allometric effects. Body weight seems to play only a minor, indirect role in the evolution of canine dimorphism. Diet plays no role. Likewise, we find little evidence that phylogenetic inertia is a constraint on the evolution of canine dimorphism.     

Patterns of dental wear and the role of the canine in Cercopithecinae.

The importance of dental wear patterns in understanding masticatory functions in primates has long been appreciated. However, studies of wear patterns among populations of nonhuman primates are few. The purpose of this investigation is to establish the developmental aspects of dental wear in the Cercopithecinae and to describe certain relevant morphological traits. Studies were made of dental casts from 200 primate specimens of Macaca nemestrina, Macaca mulatta, and Papio cynocephalus. These casts were taken at four-month intervals, beginning at two years of age and continuing over a period of six to seven years. The wear pattern starts with the rounding and eventual flattening of the protoconid and protocone of the erupted first molars. Once this stage is reached, the hypoconid and metaconid of the mandibular, and the hypocone and paracone of the maxillary molars are rounded and eventually flattened. This pattern is maintained until the cusp tips are removed and the dentin exposed, however, the entoconid and metacone are not subjected to significant wear at this stage. Analysis of these dental casts and museum specimens has provided data on the development of dental wear during the maturation of these primates. The distribution of forces acting upon the teeth produce diagnostic patterns of wear, which provide evidence of the force location and magnitude. In examining the data, the hypothesis of canine guidance and its limitation of mandibular motion was evaluated. Specimens whose canines were removed demonstrate that the canines play no significant role in the development or maintenance of dental wear planes.     

Tooth crown heights, tooth wear, sexual dimorphism and jaw growth in hominoids

The aim of this review is to bring together data that link tooth morphology with tooth function and tooth growth: We aim to show how the microanatomy of hominoid teeth is providing evidence about rates of tooth growth that are likely to be a consequence of both masticatory strategy and social behaviour. First, we present data about incisor and molar tooth wear in wild short chimpanzees that demonstrate how crown heights are likely to be related to relative tooth use in a broad sense. Following this we review recent studies that describe the microanatomy of hominoid tooth enamel and show how these studies are providing evidence about tooth crown formation times in hominoids, as well as improving estimates for the age at death of certain juvenile fossil hominids. Next, we outline what is known about the mechanisms of tooth growth in the sexually dimorphic canine teeth of chimpanzees and compare these patterns of growth with tooth growth patterns in the canines of three fossil hominids from Laetoli, Tanzania. Finally, we discuss how selection pressures that operate to increase or reduce the size of anterior teeth interact with jaw size. We argue that the space available to grow developing teeth in the mandibles of juvenile hominoids is determined by the growth patterns of the mandibles, which in turn reflect masticatory strategy. The consequences of selection pressure to grow large or small anterior teeth are likely to be reflected in the times at which these teeth are able to emerge into occlusion.     

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.     

Canine dimorphism

Canine dimorphism in many primates is exaggerated, with males possessing enormous, sharp canines that project far beyond the occlusal plane of the other teeth and females having smaller, less projecting canines. Ever since Darwin,¹ canine dimorphism generally has been attributed to sexual selection. However, recent analyses suggest that the evolution of canine dimorphism is complex and that the sexual selection hypothesis is only part of the story.     

Canine reduction in the miocene hominoid Oreopithecus bambolii: behavioural and evolutionary implications

The degree of canine size sexual dimorphism and relative canine size, which have been related to levels of agonistic behaviour amongst living anthropoid primates, together with relative molar size, are evaluated in the fossil hominoid Oreopithecus bambolii from the Late Miocene of Italy. Although Oreopithecus displays a significant degree of canine height sexual dimorphism, using allometric techniques and body mass estimates for fossil species, it is shown that Oreopithecus males are microdont (smaller postcanine as well as canine teeth than expected) when compared to most living hominoids and its putative ancestor Dryopithecus. Canine reduction in Oreopithecus includes both crown height and, especially, basal area, and most closely resembles the condition found in the pygmy chimpanzee Pan paniscus. Interestingly, it had been previously proposed that Oreopithecus displays, like pygmy chimpanzees, a paedomorphic cranial morphology resulting in a reduction of facial prognathism, which could be related to microdontia in both taxa. Independent canine reduction in several anthropoid lineages (including hominids and P. paniscus) has been related to a relaxation of the selection pressure favouring canine use as a weapon. Although changes in socio-sexual behaviour, as documented in P. paniscus, cannot be currently discarded in Oreopithecus, canine reduction could be also alternatively (although not exclusively) interpreted as an aspect of generalized microdontia. The latter is best considered an adaptive readjustment required by the paedomorphic reduction of prognathism and the resulting lack of space to accommodate the adult dentition. This mechanism of canine reduction highlights the significance of developmental constraints in evolution and had not been previously suggested for any anthropoid primate.     

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.     

Canine reduction in early man: A critique of three mechanical models

The possibility that projecting maxillary canines interfere with either a «rotary chewing» form of molar occlusion or the lateral excursion of the mandible has been used to suggest two dietary (non-weapon) selection models for canine reduction in the earliest male humans. A third model explaining canine reduction is based on the idea that a projecting mandibular canine could interfere with its tip-to-tip occlusion with the maxillary lateral incisor. In this paper, these three mechanical models are critically reexamined in light of more recent studies of occlusion in extant primates, detailed observations of anterior tooth morphology and wear in Miocene to Recent anthropoids, cheek tooth microwear inA. afarensis, and the currently accepted phylogeny and fossil record of the great apes and man.     

Multimale mating and absence of canine tooth dimorphism in woolly spider monkeys (Brachyteles arachnoides)

The relatively low degree of canine tooth dimorphism in Australopithecus afarensis has been used as “primary evidence” to support the concept of a mating system of monogamous pair-bonding and male provisioning. A recent field study of woolly spider monkeys shows that these large primates, which lack canine tooth (and body size) dimorphism, are characterized by apolygynous mating system. Male parental care of infants is absent in this species. These data support the view that a lack of canine tooth dimorphism in an anthropoid species does not necessarily imply either a monogamous, pair-bonded mating system or male parental care.     

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.     

Intrasexual competition and body weight dimorphism in anthropoid primates

Body weight dimorphism in anthropoid primates has been thought to be a consequence of sexual selection resulting from male-male competition for access to mates. However, while monogamous anthropoids show low degrees of weight dimorphism, as predicted by the sexual selection hypothesis, polygynous anthropoids show high variation in weight dimorphism that is not associated with measures of mating system or sex ratio. This observation has led many to debate the role of other factors such as dietary constraints, predation pressure, substrate constraints, allometric effects, and phylogeny in the evolution of anthropoid weight dimorphism. Here, we re-evaluate variation in adult body weight dimorphism in anthropoids, testing the sexual selection hypothesis using categorical estimates of the degree of male-male intrasexual competition (“competition levels”). We also test the hypotheses that interspecific variation in body weight dimorphism is associated with female body weight and categorical estimates of diet, substrate use, and phylogeny. Weight dimorphism is strongly associated with competition levels, corroborating the sexual selection hypothesis. Weight dimorphism is positively correlated with increasing female body weight, but evidence suggests that the correlation reflects an interaction between overall size and behavior. Arboreal species are, on average, less dimorphic than terrestrial species, while more frugivorous species tend to be more dimorphic than folivorous or insectivorous species. Several alternative hypotheses can explain these latter results. Weight dimorphism is correlated with taxonomy, but so too are competition levels. We suggest that most taxonomic correlations of weight dimorphism represent “phylogenetic niche conservatism”; however, colobines show consistently low degrees of weight dimorphism for reasons that are not clear. Am J Phys Anthropol 103:37–68, 1997. © 1997 Wiley-Liss, Inc.     

THE EVOLUTION OF PHENOTYPIC CORRELATIONS AND “DEVELOPMENTAL MEMORY”

Development introduces structured correlations among traits that may constrain or bias the distribution of phenotypes produced. Moreover, when suitable heritable variation exists, natural selection may alter such constraints and correlations, affecting the phenotypic variation available to subsequent selection. However, exactly how the distribution of phenotypes produced by complex developmental systems can be shaped by past selective environments is poorly understood. Here we investigate the evolution of a network of recurrent nonlinear ontogenetic interactions, such as a gene regulation network, in various selective scenarios. We find that evolved networks of this type can exhibit several phenomena that are familiar in cognitive learning systems. These include formation of a distributed associative memory that can “store” and “recall” multiple phenotypes that have been selected in the past, recreate complete adult phenotypic patterns accurately from partial or corrupted embryonic phenotypes, and “generalize” (by exploiting evolved developmental modules) to produce new combinations of phenotypic features. We show that these surprising behaviors follow from an equivalence between the action of natural selection on phenotypic correlations and associative learning, well‐understood in the context of neural networks. This helps to explain how development facilitates the evolution of high‐fitness phenotypes and how this ability changes over evolutionary time.     

Preliminary examination of non-occlusal dental microwear in anthropoids: Implications for the study of fossil primates

Most studies of microscopic wear on non-human primate teeth have focused on the occlusal surfaces of molars. Recent analyses of the buccal surfaces of human cheek teeth have demonstrated an association between diet and dental microwear on the these surfaces as well. In the current study, we examine microwear on both the buccal and lingual surfaces of non-human primate molars to assess the potential of these surfaces to reveal information concerning anthropoid feeding behaviors. We compare frequency of microwear occurrence in 12 extant and 11 fossil anthropoid species. Among the living primates, the occurrence of microwear on non-occlusal surfaces appears to relate to both diet and degree of terrestriality. The implications of this research for the inference of feeding behaviors and substrate use in fossil cercopithecoids are discussed. © 1996 Wiley-Liss, Inc.     

A tooth at the border of two morphogenetic fields

A tooth at the border between two morphogenetic fields (mandibular canine and honing premolar) may become morphologically similar to and/or functionally incorporated with the teeth of either field. In light of this, observations of the morphology and occlusion of female anthropoid C1s from 58 extant species are presented to assess whether and to what extent they exhibit incisor-like form and function. Female C1s in 74% of the taxa observed exhibit well developed incisor-like traits which may reflect field border phenomena. In another 9%, incisor traits are present but they are not examples of field border phenomena. Interspecies variation in female C1 morphology is related to behavior, function, natural selection and phyletic inertia. A selection model, derived from the data, is used to explain C1 sexual dimorphism and the evolution of male and female human canines. The data's relevance to the field vs clone theory debate is also discussed.     

Early hominid feeding mechanisms.

Three predominant influences mark the evolution of human head form: big brain, erect bipedalism, modified oral apparatus. Confusing interplay between different adaptive requirements of each feature has made explanation of skull structure extremely difficult in the past. It now seems possible to isolate each influence in early fossil forms. A model of mammalian modes of feeding adaptation is proposed in the form of a “Natural Experiment” for tighter analysis of fossil forms. Two forms of australopithecines are recognized, “gracile” and “robust.” Both had closely similar brains, both had erect bipedalism, but each had different masticatory construction. Separation of the first two similar influences isolates the adaptive differences in oral mechanics. The gracile form had a projecting oral apparatus, distinct canine and zygomatic buttresses, moderate jaw-lever development, jaw joint not unlike most higher primates, large unusual anterior teeth, moderately sized posterior teeth. The robust form had a retruded, greatly deepened oral apparatus, “dished-in” face with fused canine and zygomatic buttresses, powerful jaw-lever development, distinctively different joint construction, remarkably small anterior teeth, enormous posterior teeth. Striking evidence for extraordinary jaw movements emerges from these features in the robust form. This is strongly supported by remarkably close parallels in Ursidae: grizzly bear and giant panda.     

A nonadaptive dental trait

Compared to other anthropoid females, female cercopithecoids possess hypertrophied honing premolars (P₃) yet lack hypertrophied maxillary canines. In addition, female cercopithecoid maxillary canines are often tip-blunted, the crown rarely extends down to the entire shearing surface on the buccal face of P₃, and honing wear is usually confined to a small fraction of its hypertrophied buccal surface. The likely reason why the female P₃ has an unusually long buccal face is that genes involved in the expression of this morphology are also in males, for which the hypertrophied condition is adaptive—it serves as the honing surface for their hypertrophied canines. The data suggest that the hypertrophied P₃ of females is the correlated and nonadaptive response of an homologous characteristic. The possibility that this occurs in other female anthropoids and in other parts of the C/P complex is discussed, as well as the relevance of this phenomenon for understanding human canine evolution and identifying other traits which may also be examples of correlated response.     

Sex Differences in Hadza Dental Wear Patterns

Among hunter-gatherers, the sharing of male and female foods is often assumed to result in virtually the same diet for males and females. Although food sharing is widespread among the hunting and gathering Hadza of Tanzania, women were observed eating significantly more tubers than men. This study investigates the relationship between patterns of dental wear, diet, and extramasticatory use of teeth among the Hadza. Casts of the upper dentitions were made from molds taken from 126 adults and scored according to the Murphy dental attrition scoring system. Females had significantly greater anterior occlusal wear than males when we controlled for age. Males exhibited greater asymmetry in wear, with greater wear on the left side in canines, first premolars, and first molars. We suggest that these sex differences in wear patterns reflect the differences seen in the diet, as well as in the use of teeth as tools.