The adaptive significance of mandibular symphyseal fusion in mammals.

The mandibular symphyseal joint is remarkably variable across major mammalian clades, ranging in adults from unfused (amphiarthrosis) to partially fused (synarthrosis) to completely ossified (synostosis). Experimental work conducted on primates suggests that greater ossification of the symphysis is a response to increased recruitment of the balancing-side (i.e. nonchewing side) jaw-adductor muscles during forceful unilateral biting and chewing, with increased fusion strengthening the symphysis against correspondingly elevated joint stresses. It is thus expected that species with diets composed primarily of foods that require high-magnitude bite forces and/or repetitive loading to process will be characterized by greater degrees of symphyseal ossification than species with relatively easy-to-process diets (i.e. food items typified by low toughness and/or low stiffness). However, comparative support for this idea is limited. We tested this hypothesis in four dietarily diverse mammalian clades characterized by variation in symphyseal fusion - the Strepsirrhini, Marsupialia, Feliformia, and Caniformia. We scored fusion in adult specimens of 292 species, assigned each to a dietary category based on literature accounts, and tested for an association between these two variables using Pagel's test for the correlated evolution of binary characters. Results indicate that greater fusion is associated with diets composed of resistant items in strepsirrhines, marsupials, and feliforms, providing some support for the hypothesis. However, no such relationship was detected in caniforms, suggesting that factors other than dietary mechanical properties influence symphyseal ossification. Future work should focus on such factors, as well as those that favour an unfused mandibular symphysis.

Masticatory biomechanics and masseter fiber-type plasticity.

Compared to force-resisting elements of the mammalian feeding apparatus, data on jaw-muscle plasticity are less common. This hinders our understanding of the role of force-producing structures in craniofacial development and integration. Thus, we investigated fiber-type abundance and cross-sectional area in the masseter muscle of growing rabbits subjected to diet-induced variation in masticatory stresses. Three loading cohorts were obtained as weanlings and raised until adult on different diets. Immediately following euthanasia, left-sided masseters were dissected away, weighed, and then divided into anterior, intermediate and posterior sections for fiber-type immunohistochemistry. These data were compared to mandibular proportions and biomineralization from the same subjects. Results indicate that growing mammals fed a tougher, fracture-resistant diet develop: absolutely and relatively lower numbers of Type I jaw-muscle fibers; absolutely larger fiber cross-sectional areas; and relative increases in the amount of Type II fibers. These analyses indicate that an early postweaning dietary shift can induce significant variation in muscle fiber types. Such norms of reaction are comparable to those observed in bony elements. Functionally, the processing of fracture-resistant foods results in jaw adductors potentially characterized by faster contraction times and higher force production capabilities, which may influence the frequency and amplitude of forces experienced by oral tissues.

Transverse masticatory movements, occlusal orientation, and symphyseal fusion in selenodont artiodactyls.

Based on extensive experimental work on primates, two masticatory loading regimes have emerged as the likely determinants of mandibular symphyseal fusion-dorsoventral shear and lateral transverse bending (wishboning) (Ravosa and Hylander, 1994; Hylander et al., 1998, 2000). Recently, however, it has been argued that, rather than functioning to strengthen the symphysis during mastication, fusion serves to stiffen the symphyseal joint so as to facilitate increased transverse jaw movements during occlusion (Lieberman and Crompton, 2000). As part of this transverse stiffness model, it has been suggested that taxa with fused symphyses should also exhibit more horizontally oriented occlusal wear facets. Using a series of univariate and bivariate analyses, we test predictions of these three models in a sample of 44 species of selenodont artiodactyls. Consistent with the wishboning and transverse stiffness models, taxa with fused symphyses (camelids) have more horizontally oriented M(2) and M(2) occlusal wear facets, anteroposteriorly (AP) elongate symphyses, and relatively wider corpora. Contrary to the dorsoventral shear model, camelids do not have relatively deeper corpora (due to greater parasagittal bending). While taxa with ossified symphyses have relatively larger symphysis cross-sectional areas, this appears to be the byproduct of an increase in AP symphysis length due to greater lateral transverse bending of the mandible. Theoretical consideration of the biomechanics of mastication further suggests that strength, not stiffness, is the critical factor in determining symphyseal ossification. Thus, like anthropoid primates, fusion in selenodont artiodactyls appears to function in resisting increased wishboning stresses arising from an emphasis on transverse occlusal/mandibular movements and loads.

The primate cranial base: ontogeny, function, and integration.

Understanding the complexities of cranial base development, function, and architecture is important for testing hypotheses about many aspects of craniofacial variation and evolution. We summarize key aspects of cranial base growth and development in primates that are useful for formulating and testing hypotheses about the roles of the chondrocranium and basicranium in cranial growth, integration, and function in primate and human evolution. We review interspecific, experimental, and ontogenetic evidence for interactions between the cranial base and brain, and between the cranial base and the face. These interactions indicate that the cranial base plays a key role in craniofacial growth, helping to integrate, spatially and functionally, different patterns of growth in various adjoining regions of the skull such as components of the brain, the eyes, the nasal cavity, the oral cavity, and the pharynx. Brain size relative to cranial base length appears to be the dominant influence on many aspects of basicranial variation, especially the angle of the cranial base in the midsagittal plane, but other factors such as facial size, facial orientation, and posture may also be important. Major changes in cranial base shape appear to have played crucial roles in the evolution of early primates, the origin of anthropoids, and the origin of Homo sapiens.

Size and scaling in the mandible of living and extinct apes.

The purpose of this study is to fill a gap in our knowledge of dietary and allometric determinants of masticatory function and mandibular morphology in major catarrhine clades. To extend the implications of previous work on variation in mandibular form and function in other primates, a scaling analysis was performed on 20 extinct and 7 living non-cercopithecoid catarrhines or 'dental apes'. Results of allometric comparisons indicate that for a given jaw length, larger apes exhibit significantly more robust corpora and symphyses than smaller forms. This appears linked to size-related increases in dietary toughness and/or hardness, which in turn causes elevated mandibular loads and/or greater repetitive loading during unilateral mastication. Larger-bodied dental apes also display more curved symphyses, which also explains the positive allometry of symphysis width and height. In apes, proconsulids often evince more robust jaws while all hylobatids, Pan and Dryopithecus laietanus possess more gracile cross sections. In propliopithecids, Aegyptopithecus is always more robust than Propliopithecus. In proconsulids, Rangwapithecus and Micropithecus commonly exhibit more robust jaws whereas Dendropithecus and especially Simiolus are more gracile. Most of the larger taxa are folivorous and/or hard-object frugivorous pongids with relatively larger dentaries. Though apes have relatively wider corpora than cercopithecines due to greater axial twisting of the corpora during chewing, they are otherwise alike in robusticity levels. Smaller apes are similar to cercopithecines in evincing a relatively high degree of symphyseal curvature, while larger taxa are like colobines in having less curvature. Larger pongids resemble or even exceed colobine jaw proportions and thus appear to converge on colobines in terms of the mechanical properties of their diets.

Remarkable species diversity in Malagasy mouse lemurs (primates, Microcebus).

Phylogenetic analysis of mtDNA sequence data confirms the observation that species diversity in the world's smallest living primate (genus Microcebus) has been greatly underestimated. The description of three species new to science, and the resurrection of two others from synonymy, has been justified on morphological grounds and is supported by evidence of reproductive isolation in sympatry. This taxonomic revision doubles the number of recognized mouse lemur species. The molecular data and phylogenetic analyses presented here verify the revision and add a historical framework for understanding mouse lemur species diversity. Phylogenetic analysis revises established hypotheses of ecogeographic constraint for the maintenance of species boundaries in these endemic Malagasy primates. Mouse lemur clades also show conspicuous patterns of regional endemism, thereby emphasizing the threat of local deforestation to Madagascar's unique biodiversity.

Symphyseal fusion and jaw-adductor muscle force: an EMG study.

The purpose of this study is to test various hypotheses about balancing-side jaw muscle recruitment patterns during mastication, with a major focus on testing the hypothesis that symphyseal fusion in anthropoids is due mainly to vertically- and/or transversely-directed jaw muscle forces. Furthermore, as the balancing-side deep masseter has been shown to play an important role in wishboning of the macaque mandibular symphysis, we test the hypothesis that primates possessing a highly mobile mandibular symphysis do not exhibit the balancing-side deep masseter firing pattern that causes wishboning of the anthropoid mandible. Finally, we also test the hypothesis that balancing-side muscle recruitment patterns are importantly related to allometric constraints associated with the evolution of increasing body size. Electromyographic (EMG) activity of the left and right superficial and deep masseters were recorded and analyzed in baboons, macaques, owl monkeys, and thick-tailed galagos. The masseter was chosen for analysis because in the frontal projection its superficial portion exerts force primarily in the vertical (dorsoventral) direction, whereas its deep portion has a relatively larger component of force in the transverse direction. The symphyseal fusion-muscle recruitment hypothesis predicts that unlike anthropoids, galagos develop bite force with relatively little contribution from their balancing-side jaw muscles. Thus, compared to galagos, anthropoids recruit a larger percentage of force from their balancing-side muscles. If true, this means that during forceful mastication, galagos should have working-side/balancing-side (W/B) EMG ratios that are relatively large, whereas anthropoids should have W/B ratios that are relatively small. The EMG data indicate that galagos do indeed have the largest average W/B ratios for both the superficial and deep masseters (2.2 and 4.4, respectively). Among the anthropoids, the average W/B ratios for the superficial and deep masseters are 1.9 and 1.0 for baboons, 1.4 and 1.0 for macaques, and both values are 1.4 for owl monkeys. Of these ratios, however, the only significant difference between thick-tailed galagos and anthropoids are those associated with the deep masseter. Furthermore, the analysis of masseter firing patterns indicates that whereas baboons, macaques and owl monkeys exhibit the deep masseter firing pattern associated with wishboning of the macaque mandibular symphysis, galagos do not exhibit this firing pattern. The allometric constraint-muscle recruitment hypothesis predicts that larger primates must recruit relatively larger amounts of balancing-side muscle force so as to develop equivalent amounts of bite force. Operationally this means that during forceful mastication, the W/B EMG ratios for the superficial and deep masseters should be negatively correlated with body size. Our analysis clearly refutes this hypothesis. As already noted, the average W/B ratios for both the superficial and deep masseter are largest in thick-tailed galagos, and not, as predicted by the allometric constraint hypothesis, in owl monkeys, an anthropoid whose body size is smaller than that of thick-tailed galagos. Our analysis also indicates that owl monkeys have W/B ratios that are small and more similar to those of the much larger-sized baboons and macaques. Thus, both the analysis of the W/B EMG ratios and the muscle firing pattern data support the hypothesis that symphyseal fusion and transversely-directed muscle force in anthropoids are functionally linked. This in turn supports the hypothesis that the evolution of symphyseal fusion in anthropoids is an adaptation to strengthen the symphysis so as to counter increased wishboning stress during forceful unilateral mastication. (ABSTRACT TRUNCATED)

Evolution of anthropoid jaw loading and kinematic patterns.

Major transformations in the skull and masticatory system characterized the evolution of crown anthropoids. To offer further insight into the phylogenetic and arguably adaptive significance of specific primate mandibular loading and kinematic patterns, allometric analyses of metric parameters linked to masticatory function are performed within and between 47 strepsirhine and 45 recent anthropoid species. When possible, basal anthropoids are considered. These results are subsequently integrated with prior experimental and morphological work on primate skull form. As compared to strepsirhines, crown anthropoids have a vertically longer ascending ramus linked to a glenoid and condyle positioned relatively higher above the occlusal plane. Interestingly, anthropoids and strepsirhines do not exhibit different mean ratios of condylar to glenoid height, which suggests that both clades are similar in their ability to evenly distribute occlusal contacts and perhaps forces along the postcanine teeth. Thus, given the considerable suborder differences in the scaling of both glenoid and condylar height, we argue that much of this variation in jaw-joint height is linked to suborder differences in relative facial height due in turn to increased encephalization, basicranial flexion, and facial kyphosis in anthropoids. Due to a more elongate ascending ramus, anthropoids evince more vertically oriented masseters than like-sized strepsirhines. Having a relatively longer ramus and a more medially displaced lateral pterygoid plate, crown anthropoids exhibit medial pterygoids oriented similar to those of strepsirhines, but with a variably longer lever arm. As anthropoid masseters are less advantageously placed to effect transverse movements/forces, we argue that balancing-side deep-masseter activity underlying a wishboning loading regime serves to increase, or at least maintain, transverse levels of jaw movement and occlusal force at the end of the masticatory power stroke. Crown anthropoids are also more isognathic and isodontic than strepsirhines. A consideration of early anthropoids suggests that the crown anthropoid masticatory pattern, i.e., more vertical masseters due to a high condyle as well as greater isognathy and isodonty, occurred stepwise during stem anthropoid evolution. This appears to correspond to a more transverse, and perhaps progressively larger, power stroke across oligopithecids, parapithecids, and propliopithecids.

Strain in the galago facial skull.

Little experimental work has been directed at understanding the distribution of stresses along the facial skull during routine masticatory behaviors. Such information is important for understanding the functional significance of the mammalian circumorbital region. In this study, bone strain was recorded along the dorsal interorbit, postorbital bar, and mandibular corpus in Otolemur garnettii and O. crassicaudatus (greater galagos) during molar chewing and biting. We determined principal-strain magnitudes and directions, compared peak shear-strain magnitudes between various regions of the face, and compared galago strain patterns with similar experimental data for anthropoids. This suite of analyses were used to test the facial torsion model (Greaves [1985] J Zool (Lond) 207:125-136; [1991] Zool J Linn Soc 101:121-129; [1995] Functional morphology in vertebrate paleontology. Cambridge: Cambridge University Press, p 99-115). A comparison of galago circumorbital and mandibular peak strains during powerful mastication indicates that circumorbital strains are very low in magnitude. This demonstrates that, as in anthropoids, the strepsirhine circumorbital region is highly overbuilt for countering routine masticatory loads. The fact that circumorbital peak-strain magnitudes are uniformly low in both primate suborders undermines any model that emphasizes the importance of masticatory stresses as a determinant of circumorbital form, function, and evolution. Preliminary data also suggest that the difference between mandibular and circumorbital strains is greater in larger-bodied primates. This pattern is interpreted to mean that sufficient cortical bone must exist in the circumorbital region to prevent structural failure due to nonmasticatory traumatic forces. During unilateral mastication, the direction of epsilon(1) at the galago dorsal interorbit indicates the presence of facial torsion combined with bending in the frontal plane. Postorbital bar principal-strain directions during mastication are oriented, on average, very close to 45 degrees relative to the skull's long axis, much as predicted by the facial torsion model. When chewing shifts from one side of the face to the other, there is a characteristic reversal or flip-flop in principal-strain directions for both the interorbit and postorbital bar. Although anthropoids also exhibit an interorbital reversal pattern, peak-strain directions for this clade are opposite those for galagos. The presence of such variation may be due to suborder differences in relative balancing-side jaw-muscle force recruitment. Most importantly, although the strain-direction data for the galago circumorbital region offer support for the occurrence of facial torsion, the low magnitude of these strains suggests that this loading pattern may not be an important determinant of circumorbital morphology.

Masticatory stress, orbital orientation and the evolution of the primate postorbital bar.

A postorbital bar is one of a suite of derived features which distinguishes basal primates from their putative sister taxon, plesiadapiforms. Two hypotheses have been put forward to explain postorbital bar development and variation in circumorbital form: the facial torsion model and visual predation hypothesis. To test the facial torsion model, we employ strain data on circumorbital and mandibular loading patterns in representative primates with a postorbital bar and masticatory apparatus similar to basal primates. To examine the visual predation hypothesis, we employ metric data on orbit orientation in Paleocene and Eocene primates, as well as several clades of visual predators and foragers that vary interspecifically in postorbital bar formation.A comparison of galago circumorbital and mandibular peak strains during powerful mastication demonstrates that circumorbital strains are quite low. This indicates that, as in anthropoids, the strepsirhine circumorbital region is excessively overbuilt for countering routine masticatory loads. The fact that circumorbital peak-strain levels are uniformly low in both primate suborders undermines any model which posits that masticatory stresses are determinants of circumorbital form, function and evolution. This is interpreted to mean that sufficient cortical bone must exist to prevent structural failure due to non-masticatory traumatic forces. Preliminary data also indicate that the difference between circumorbital and mandibular strains is greater in larger taxa.Comparative analyses of several extant analogs suggest that the postorbital bar apparently provides rigidity to the lateral orbital margins to ensure a high level of visual acuity during chewing and biting. The origin of the primate postorbital bar is linked to changes in orbital convergence and frontation at smaller sizes due to nocturnal visual predation and increased encephalization. By incorporating in vivo and fossil data, we reformulate the visual predation hypothesis of primate origins and thus offer new insights into major adaptive transformations in the primate skull.

Anthropoid origins and the modern symphysis.

To highlight adaptive transformations in craniomandibular form during anthropoid origins, symphyseal character states and underlying masticatory loading regimes were investigated vis-à-vis shifts in diet and body size. A study of fossil anthropoids is possible because variation in symphyseal fusion is continuous and directly proportional to the amount of symphyseal stress and because such variation can be considered a series of discrete character states each with unique functional underpinnings. Using recent systematic renderings of Eocene and Oligocene taxa as a template with which to assess character evolution, this analysis indicates when, and in which clade(s), specific masticatory features became fixed and thus diagnostic. A general trend throughout early anthropoid evolution is for descendent taxa to be progressively larger than ancestral forms. Coupled with this pattern is the tendency for larger-bodied fossil anthropoids to have ingested tougher diets variably consisting of thick-coated, unripe fruits and/or leaves. Mastication of mechanically tougher foods entails greater repetitive loading of the mandible and requires relatively larger amounts of balancing-side muscle force, thus resulting in correspondingly greater symphyseal fusion due to elevated dorsoventral shear. With a single exception, these adaptive transformations characterize the evolutionary pathway leading both to parapithecines and a catarrhine:platyrrhine clade (crown anthropoids). While the ancestor of crown anthropoids would have possessed a body size, diet and masticatory adaptations similar to parapithecines, such a common suite of features evolved independently. Moreover, the evolution of an early-fusing symphysis and associated wishboning loading regime of catarrhines and platyrrhines is unique among all anthropoids. Lastly, the apparent lack of reversals in symphyseal fusion indicates the improbability of phylogenetic hypotheses in which a relationship is proposed between 'ancestral' taxa with a greater degree of symphyseal fusion and 'descendent' anthropoids with a lesser degree of ossification.

Mandibular corpus strain in primates: further evidence for a functional link between symphyseal fusion and jaw-adductor muscle force.

Previous work indicates that compared to adult thick-tailed galagos, adult long-tailed macaques have much more bone strain on the balancing-side mandibular corpus during unilateral isometric molar biting (Hylander [1979a] J. Morphol. 159:253-296). Recently we have confirmed in these same two species the presence of similar differences in bone-strain patterns during forceful mastication. Moreover, we have also recorded mandibular bone strain patterns in adult owl monkeys, which are slightly smaller than the galago subjects. The owl monkey data indicate the presence of a strain pattern very similar to that recorded for macaques, and quite unlike that recorded for galagos. We interpret these bone-strain pattern differences to be importantly related to differences in balancing-side jaw-adductor muscle force recruitment patterns. That is, compared to galagos, macaques and owl monkeys recruit relatively more balancing-side jaw-adductor muscle force during forceful mastication. Unlike an earlier study (Hylander [1979b] J. Morphol. 160:223-240), we are unable to estimate the actual amount of working-side muscle force relative to balancing-side muscle force (i.e., the W/B muscle force ratio) in these species because we have no reliable estimate of magnitude, direction, and precise location of the bite force during mastication. A comparison of the mastication data with the earlier data recorded during isometric molar biting, however, supports the hypothesis that the two anthropoids have a small W/B jaw-adductor muscle force ratio in comparison to thick-tailed galagos. These data also support the hypothesis that increased recruitment of balancing-side jaw-adductor muscle force in anthropoids is functionally linked to the evolution of symphyseal fusion or strengthening. Moreover, these data refute the hypothesis that the recruitment pattern differences between macaques and thick-tailed galagos are due to allometric factors. Finally, although the evolution of symphyseal fusion in primates may be linked to increased stress associated with increased balancing-side muscle force, it is currently unclear as to whether the increased force is predominately vertically directed, transversely directed, or is a near equal combination of these two force components (cf. Ravosa and Hylander [1994] In Fleagle and Kay [eds.]: Anthropoid Origins. New York: Plenum, pp. 447-468).

Cranial allometry and geographic variation in slow lorises (Nycticebus)

A series of 20 craniodental measurements was obtained for two sister taxa: Nycticebus coucang (common slow loris) and N. pygmaeus (pygmy slow loris). Multivariate analysis of variance was performed with adult data to describe patterns of subspecific and specific variation in this genus. The geometric mean of adult cranial dimensions was compared to field data on latitudinal coordinates for available specimens to investigate if size variation in Nycticebus is clinal in nature. Ontogenetic series for larger-bodied N. coucang and smaller-bodied N. pygmaeus were compared to test the hypothesis that species and subspecific variation in skull form results from the differential extension of common patterns of relative growth. A MANOVA provides independent support of Groves's [pp. 44-53 in Proceedings of the Third International Congress on Primatology, Vol. 1 (Basel: S. Karger), in 1971)] classification of Nycticebus into two species, with four subspecies in the common slow loris and one form of the pygmy slow loris. Within N. coucang, cranial proportions for all four subspecies are ontogenetically scaled, and size differentiation is mainly clinal (Bergmann's Rule). N. c. bengalensis represents the most northerly disposed and the largest form. N. c. javanicus represents the next-largest form and is located in a southerly direction the next-farthest away from the equator. N. c. coucang and N. c. menagensis are both equatorial; however, the latter subspecies is the smallest. A genetic basis for some of the taxonomic variation between N. c. coucang and N. c. menagensis is supported by such nonclinal variation in body size. Variation in the presence/absence of I2 is not size-related but rather tracks geographic proximity and isolating factors which predate the most recent inundation of the Sunda Shelf. Although they inhabit a nonequatorial environment, pygmy slow lorises are the smallest of all Nycticebus. As N. pygmaeus is sympatric with N. c. bengalensis, the largest slow loris, it appears that the evolution of its smaller body size represents a case of character displacement. Unlike N. coucang, skull size becomes significantly smaller in more northern N. pygmaeus. This may also reflect character displacement between sympatric sister taxa underlain by a cline-dependent ecological factor which is marked in more northerly latitudes. On the other hand, the negative correlation between body size and latitude in N. pygmaeus could be due to the influence of nonprimate fauna, such as predators, which themselves evince a similar clinal pattern. Analyses of relative growth indicate that skull proportions in the two species of Nycticebus are ontogenetically scaled in two-thirds of the cases. All but one of the seven comparisons (interorbital breadth) which do not indicate ontogenetic scaling represent part of the masticatory complex. This likely reflects a reorganization of N. pygmaeus maxillomandibular proportions linked to smaller size and changes in diet.

Ontogeny, function, and scaling of the mandibular symphysis in papionin primates.

In vivo study of mastication in adult cercopithecine primates demonstrates a link between mandibular symphyseal form and resistance to "wishboning," or lateral transverse bending. Mechanical consideration of wishboning at the symphysis indicates exponentially higher stresses along the lingual surface with increasing symphyseal curvature. Lengthening the anteroposterior width of the symphysis acts to resist these higher loads. Interspecific adult cercopithecine allometries show that both symphyseal curvature and symphyseal width exhibit positive allometry relative to body mass. The experimental and allometric data support an hypothesis that the cercopithecine mandibular symphysis is designed to maintain functional equivalence--in this case dynamic strain similarity--in wishboning stress and strain magnitudes across adult cercopithecines. We test the hypothesis that functional equivalence during masticatory wishboning is maintained throughout ontogeny by calculating relative stress estimates from morphometric dimensions of the mandibular symphysis in two cercopithecine primates, Macaca fascicularis and M. nemestrina. Results indicate no significant differences in relative stress estimates among the two macaque ontogenies and an interspecific sample of adult papionin primates. Further, relative stress estimates do not change significantly throughout ontogeny in either species. These results offer the first evidence for the maintenance of functional equivalence in stress and strain levels during postnatal growth in a habitually loaded cranial structure. Scaling analyses demonstrate significant slope differences for both symphyseal curvature and width between the ontogenetic and interspecific samples. The distinct interspecific cercopithecine slopes are realized by a series of ontogenetic transpositions in both symphyseal curvature and width. Throughout papionin ontogeny, symphyseal curvature increases with less negative allometry, while symphysis width increases with less positive allometry versus the interspecific pattern. As symphyseal curvature and width are inversely proportional to one another in estimating relative stresses, functionally equivalent stress levels are maintained both ontogenetically and interspecifically, because the relatively slower rate of allometric increase in symphyseal curvature during growth is compensated for by a slower rate of allometric increase in symphyseal width. These results indicate the primacy of maintaining functional equivalence during growth and the need for ontogenetic data in understanding the evolutionary processes that affect form-function relations as well as the interspecific patterning of adult form across a clade.

Metastatic dissemination of human ovarian epithelial carcinoma is promoted by alpha2beta1-integrin-mediated interaction with type I collagen.

Metastatic dissemination of epithelial ovarian carcinoma is thought to be mediated via tumor cell exfoliation into the peritoneal cavity, followed by adhesion to and invasion through the mesothelium which overlies the contents of the peritoneal cavity. In this study, we have utilized short-term primary cultures to analyze the effect of specific extracellular matrix proteins on properties of human ovarian epithelial carcinoma cells which contribute to the invasive phenotype. Analysis of cell:matrix adhesive profiles indicated that ovarian carcinoma cells adhere preferentially to type I collagen. Immunoprecipitation analyses demonstrated the presence of the collagen-binding alpha2beta1 integrin in biotin-labeled ovarian carcinoma cell membranes, and cellular adhesion was inhibited by blocking antibodies directed against the alpha2 and beta1 integrin subunits. The alpha2beta1-binding peptide Asp-Gly-Glu-Ala (DGEA) was also moderately effective at blocking adhesion to collagen relative to the control peptide Ala-Gly-Glu-Ala (AGEA). Analysis of cell motility on protein-coated colloidal gold coverslips demonstrated that ovarian carcinoma cells migrate preferentially on type I collagen coated surfaces. Type I collagen promoted migration in a concentration-dependent, saturable manner, with maximal migration observed at a collagen-coating concentration of 50 microg/ml. Migration on collagen was inhibited by antibodies directed against the alpha2 and beta1 integrin subunits and by DGEA peptide, providing evidence for the role of the alpha2beta1 integrin in ovarian carcinoma cell motility. Culturing ovarian carcinoma cells on type I collagen gels led to a significant increase in conversion of the matrix metalloproteinase 2 zymogen to the 66-kD form, suggesting that adhesion to collagen also influences matrix-degrading proteinases. These data suggest that alpha2beta1-integrin-mediated interaction of ovarian carcinoma cells with type I collagen, a protein prevalent both in the mesothelial extracellular matrix and in the peritoneal cavity of ovarian carcinoma patients, may function on multiple levels to promote metastatic dissemination of ovarian carcinoma cells.

Mandibular form and function in North American and European Adapidae and Omomyidae.

Previous experimental and comparative studies among a wide variety of primate and nonprimate mammals provide a unique source of information for investigating the functional and phylogenetic significance of variation in the masticatory apparatus of Eocene primates. To provide a quantitative study of mandibular form and function in Eocene primates, the scaling of jaw dimensions and the development of symphyseal fusion was considered in a broad sample of North American and European Adapidae and Omomyidae. Statistical analyses indicate a significant size-related pattern of symphyseal fusion across Eocene primates, with larger taxa often having a greater degree of fusion than smaller species; this trend is also evident at the family level. As adapids are mostly larger than omomyids and these taxa show allometry of symphyseal fusion, this may explain why no omomyids evince complete fusion. Controlling for jaw size, species with greater symphyseal fusion tend to have more robust jaws than those with a lesser amount of fusion. Upon further examination, a primary reason why adapids have more robust mandibles than omomyids is associated with the presence of taxa with fused symphyses, and thus more robust jaws, in the adapid sample, whereas no omomyids have fused symphyses. In addition, there is little indication of a dietary effect, as measured by molar shear-crest development, on symphyseal fusion. Moreover, as there is no correlation between molar shear-crest development and skull size, this also points to the absence of a size-related pattern of dietary preference underlying the allometry of symphyseal fusion. Based on the interspecific and ontogenetic allometry of symphyseal ossification in Eocene primates, jaw-scaling patterns are used to further examine the functional determinants of fusion in this group. This study indicates that greater dorsoventral shear during mastication is a more likely factor than lateral transverse bending ("wishboning") in the evolution of symphyseal fusion among "late-fusing" mammals like adapids and omomyids. Given that wishboning is an important functional determinant of symphyseal form in recent anthropoids, apparently the evolutionary development of marked wishboning occurs only in taxa that shift the timing of fusion to a growth stage preceding the onset of weaning (before adult masticatory patterns are fully developed) and perhaps first ossified the symphysis to counter elevated dorsoventral shear stress. As early anthropoids probably consisted of members varying interspecifically and ontogenetically in the degree of ossification, it is especially informative to analyze the adaptive setting in which anthropoid symphyseal fusion evolved from a similar primitive "prosimian" perspective. Finally, since taxa with fused symphyses are widely distributed across mammals, a similar analytical framework could be directed profitably at unraveling the functional and evolutionary significance of symphyseal fusion in other mammalian clades.

Mandibular growth and function in Archaeolemur.

Ontogenetic changes in the morphology of the mandibular symphysis are described in Archaeolemur so as to infer the functional significance of symphyseal fusion in this subfossil Malagasy lemur. The first regions of the symphysis to show a more complex morphology were the lower and anterior borders of the joint and, to a lesser extent, the lingual borders of the superior and inferior transverse tori. During growth, these regions became increasingly rugose and encroached upon a centrally located, smooth, "oval" region, which may have been a principal pathway for neurovascular structures communicating with the unfused joint. In subadults, the symphysis was completely fused except for the lingual surface of the inferior transverse torus, where a patent suture and potential space were present between dentaries. Thus, in Archaeolemur there was an age- and size-related pattern of increased symphyseal ossification or fusion that was complete by adulthood. The morphology of the interlocking bony processes and the sequence of ossification in the symphysis suggest that increased dorsoventral shear stress during mastication was the most likely determinant of symphyseal fusion in Archaeolemur. The allometric pattern of greater symphyseal fusion may be linked to the presence of relatively greater dorsoventral shear in adults due to an increased recruitment of balancing-side jaw-muscle force. There is little indication that the symphysis of juvenile Archaeolemur was buttressed to resist forces associated with "wishboning" during mastication or vertical bending during incision. Our observations, as well as those of others, suggest that symphyseal fusion in primates occurs initially as a response to increased dorsoventral shear during mastication. Therefore, wishboning stress might only become a major determinant of symphyseal form and function in those taxa that develop a fused symphysis to counter increased dorsoventral shear.

Relative growth of the limbs and trunk in sifakas: heterochronic, ecological, and functional considerations.

Limb, trunk, and body weight measurements were obtained for growth series of Milne-Edwards's diademed sifaka, Propithecus diadema edwardsi, and the golden-crowned sifaka, Propithecus tattersalli. Similar measures were obtained also for primarily adults of two subspecies of the western sifaka: Propithecus verreauxi coquereli, Coquerel's sifaka, and Propithecus verreauxi verreauxi, Verreaux's sifaka. Ontogenetic series for the larger-bodied P. d. edwardsi and the smaller-bodied P. tattersalli were compared to evaluate whether species-level differences in body proportions result from the differential extension of common patterns of relative growth. In bivariate plots, both subspecies of P. verreauxi were included to examine whether these taxa also lie along a growth trajectory common to all sifakas. Analyses of the data indicate that postcranial proportions for sifakas are ontogenetically scaled, much as demonstrated previously with cranial dimensions for all three species (Ravosa, 1992). As such, P. d. edwardsi apparently develops larger overall size primarily by growing at a faster rate, but not for a longer duration of time, than P. tattersalli and P. verreauxi; this is similar to results based on cranial data. A consideration of Malagasy lemur ecology suggests that regional differences in forage quality and resource availability have strongly influenced the evolutionary development of body-size variation in sifakas. On one hand, the rainforest environment of P. d. edwardsi imposes greater selective pressures for larger body size than the dry-forest environment of P. tattersalli and P. v. coquereli, or the semi-arid climate of P. v. verreauxi. On the other hand, as progressively smaller-bodied adult sifakas are located in the east, west, and northwest, this apparently supports suggestions that adult body size is set by dry-season constraints on food quality and distribution (i.e., smaller taxa are located in more seasonal habitats such as the west and northeast). Moreover, the fact that body-size differentiation occurs primarily via differences in growth rate is also due apparently to differences in resource seasonality (and juvenile mortality risk in turn) between the eastern rainforest and the more temperate northeast and west. Most scaling coefficients for both arm and leg growth range from slight negative allometry to slight positive allometry. Given the low intermembral index for sifakas, which is also an adaptation for propulsive hindlimb-dominated jumping, this suggests that differences in adult limb proportions are largely set prenatally rather than being achieved via higher rates of postnatal hindlimb growth.(ABSTRACT TRUNCATED AT 400 WORDS)

Basicranial flexion, relative brain size, and facial kyphosis in nonhuman primates.

Numerous hypotheses explaining interspecific differences in the degree of basicranial flexion have been presented. Several authors have argued that an increase in relative brain size results in a spatial packing problem that is resolved by flexing the basicranium. Others attribute differences in the degree of basicranial flexion to different postural behaviors, suggesting that more orthograde animals require a ventrally flexed pre-sella basicranium in order to maintain the eyes in a correct forward-facing orientation. Less specific claims are made for a relationship between the degree of basicranial flexion and facial orientation. In order to evaluate these hypotheses, the degree of basicranial flexion (cranial base angle), palate orientation, and orbital axis orientation were measured from lateral radiographs of 68 primate species and combined with linear and volumetric measures as well as data on the size of the neocortex and telencephalon. Bivariate correlation and partial correlation analyses at several taxonomic levels revealed that, within haplorhines, the cranial base angle decreases with increasing neurocranial volume relative to basicranial length and is positively correlated with angles of facial kyphosis and orbital axis orientation. Strepsirhines show no significant correlations between the cranial base angle and any of the variables examined. It is argued that prior orbital approximation in the ancestral haplorhine integrated the medial orbital walls and pre-sella basicranium into a single structural network such that changes in the orientation of one necessarily affect the other. Gould's ("Ontogeny and Phylogeny." Cambridge: Belknap Press, 1977) hypothesis, that the highly flexed basicranium of Homo may be due to a combination of a large brain and a relatively short basicranium, is corroborated.