Matthew J. Ravosa

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)

Structural allometry of the prosimian mandibular corpus and symphysis

Abstract Experimental and comparative studies among primates suggest that symphyseal fusion and relatively large mandibular symphysis and corpus dimensions are often part of the same functional pattern Hylander, 1977 , Hylander, 1979a , Hylander, 1979b , Hylander, 1984 , Hylander, 1985 , Hylander, 1988 ; Beecher, 1977 , Beecher, 1979 , Beecher, 1983 . To test this hypothesis further, the biomechanical scaling of corpus and symphysis dimensions was examined in prosimians and compared to anthropoids. Symphyseal fusion was similarly investigated in large-bodied Malagasy “subfossil” lemurs. Dietary influences on prosimian corpus and symphysis proportions were also considered, because leaf-eating positively affects the degree of symphyseal fusion ( Beecher, 1977 , Beecher, 1979 , Beecher, 1983 ; but see also Greaves, 1988 and mandibular robusticity ( Hylander, 1979a ; Bouvier, 1986a , Bouvier, 1986b ). Prosimian regression lines for mandibular corpus and symphysis measures are significantly transposed below those for anthropoids.Palaeopropithecus maximus, P. ingens, Hadropithecus stenognathus, Archaeolemur edwardsi andA. majori display relatively robust symphysis and corpus dimensions, which appear to be related to large body size and folivory.Megaladapis madagascariensis, M. grandidieri andM. edwardsi have more moderately positive residuals; thus symphyseal fusion appears more singularly the result of large size. Leaf-eating prosimians, such as indriids, do display relatively large corpora and symphyses. These data strongly support previous predictions about structural and functional differences between the masticatory system of extant primate suborders (e.g., Hylander, 1979a ; Beecher, 1977 , Beecher, 1979 ).

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).

Effects of brain and facial size on basicranial form in human and primate evolution

Understanding variation in the basicranium is of central importance to paleoanthropology because of its fundamental structural role in skull development and evolution. Among primates, encephalisation is well known to be associated with flexion between midline basicranial elements, although it has been proposed that the size or shape of the face influences basicranial flexion. In particular, brain size and facial size are hypothesized to act as antagonists on basicranial flexion. One important and unresolved problem in hominin skull evolution is that large-brained Neanderthals and some Mid-Pleistocene humans have slightly less flexed basicrania than equally large-brained modern humans. To determine whether or not this is a consequence of differences in facial size, geometric morphometric methods were applied to a large comparative data set of non-human primates, hominin fossils, and humans (N=142; 29 species). Multiple multivariate regression and thin plate spline analyses suggest that basicranial evolution is highly significantly influenced by both brain size and facial size. Increasing facial size rotates the basicranium away from the face and slightly increases the basicranial angle, whereas increasing brain size reduces the angles between the spheno-occipital clivus and the presphenoid plane, as well as between the latter and the cribriform plate. These interactions can explain why Neanderthals and some Mid-Pleistocene humans have less flexed cranial bases than modern humans, despite their relatively similar brain sizes. We highlight that, in addition to brain size (the prime factor implicated in basicranial evolution in Homo), facial size is an important influence on basicranial morphology and orientation. To better address the multifactorial nature of basicranial flexion, future studies should focus on the underlying factors influencing facial size evolution in hominins.

PRIMATE ORIGINS: Adaptations and evolution

Supraordinal Relationships of Primates and Their Time of Origin.- A Molecular Classification for the Living Orders of Placental Mammals and the Phylogenetic Placement of Primates.- New Light on the Dates of Primate Origins and Divergence.- The Postcranial Morphology of Ptilocercus lowii (Scandentia, Tupaiidae) and its Implications for Primate Supraordinal Relationships.- Primate Origins: A Reappraisal of Historical Data Favoring Tupaiid Affinities.- Primate Taxonomy, Plesiadapiforms, and Approaches to Primate Origins.- Adaptations and Evolution of the Cranium.- Jaw-Muscle Function and the Origin of Primates.- Were Basal Primates Nocturnal? Evidence From Eye and Orbit Shape.- Oculomotor Stability and the Functions of the Postorbital Bar and Septum.- Primate Origins and the Function of the Circumorbital Region: Whats Load Got to Do with It?.- Adaptations and Evolution of the Postcranium.- Origins of Grasping and Locomotor Adaptations in Primates: Comparative and Experimental Approaches Using an Opossum Model.- Evolvability, Limb Morphology, and Primate Origins.- Primate Gaits and Primate Origins.- Morphological Correlates of Forelimb Protraction in Quadrupedal Primates.- Ancestral Locomotor Modes, Placental Mammals, and the Origin of Euprimates: Lessons From History.- The Postcranial Morphotype of Primates.- New Skeletons of Paleocene-Eocene Plesiadapiformes: A Diversity of Arboreal Positional Behaviors in Early Primates.- Adaptations and Evolution of the Brain, Behavior, Physiology, and Ecology.- Start Small and Live Slow: Encephalization, Body Size, and Life History Strategies in Primate Origins and Evolution.- Evolutionary Specializations of Primate Brain Systems.- New Views on the Origin of Primate Social Organization.- Primate Bioenergetics: An Evolutionary Perspective.- Episodic Molecular Evolution of Some Protein Hormones in Primates and Its Implications for Primate Adaptation.- Parallelisms Among Primates and Possums.- Perspectives on Primate Color Vision.

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 ϵ1 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° relative to the skulls 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. J. Morphol. 245:51–66, 2000

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.

Jaw morphology and function in living and fossil old world monkeys

This allometric investigation on a sample of 29 cercopithecine and 22 colobine taxa augments the data and implications of prior work on subfamilial variation in mandibular form and function in recent Cercopithecidae. To increase the size range encompassed by living cercopithecines and colobines, I included many of the larger-bodied fossil specimens. These analyses serve to fill a gap in our understanding of size-related changes in masticatory function and symphyseal morphology and curvature in extant and extinct Old World monkeys. Results of subfamilial scaling comparisons indicate that for a given jaw length, colobines possess significantly more robust corpora and symphyses than those of cercopithecines, especially at smaller sizes. Following from previous work, the most plausible explanation for why the subfamilies differ in relative corporeal and symphyseal dimensions is that colobine mandibles experience elevated loads and greater repetitive loading during mastication due, on average, to processing a diet of tough leaves and/or seeds. Although colobines have relatively larger symphyses, subfamilial analyses of symphyseal curvature demonstrate that they evince less symphyseal curvature vis-à-vis cercopithecines of a common size. Moreover, both subfamilies exhibit similar allometric changes in the degree of curvature, such that larger-bodied Old World monkeys have more curved symphyses than those of smaller taxa. Subfamilial scaling analyses also indicate that colobines possess a shorter M2 bite-point length relative to masseter lever-arm length, but not versus temporalis lever-arm length. Thus, as compared to cercopithecines, colobines can recruit less masseter-muscle force to produce similar bite forces during mastication. In both clades, M2 bite-point length scales with positive allometry relative to masseter lever-arm length, such that larger species are less efficient at generating molar bite forces. This seems especially important due to the lack of subfamily difference in M2 bite-point:temporalis lever-arm scaling (which is isometric across cercopithecids). A consideration of extinct cercopithecids indicates that many of the large-bodied papionins have more robust corpora, due perhaps to a diet which was of similar toughness to that of extant and extinct colobines. However, the biomechanical arrangements of the masseter and temporalis in all but one fossil cercopithecine and all of the fossil colobine specimens are much as predicted for a subfamilial member of its skull size. That most large-bodied papionins with tougher diets nonetheless maintain a less efficient jaw-muscle configuration may be due to stronger offsetting selection for increased relative canine size and gape.

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.

Metastatic Dissemination of Human Ovarian Epithelial Carcinoma Is Promoted by α2β1-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 α2β1 integrin in biotin-labeled ovarian carcinoma cell membranes, and cellular adhesion was inhibited by blocking antibodies directed against the α2 and β1 integrin subunits. The α2β1-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 μg/ml. Migration on collagen was inhibited by antibodies directed against the α2 and β1 integrin subunits and by DGEA peptide, providing evidence for the role of the α2β1 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 α2β1-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.