scispace - formally typeset
Search or ask a question
Journal ArticleDOI

Pushing the limit: masticatory stress and adaptive plasticity in mammalian craniomandibular joints

TL;DR: It is argued that a critical component of current and future research on adaptive plasticity in the skull, and especially cranial joints, should employ a multifaceted characterization of a functional system, one that incorporates data on myriad tissues so as to evaluate the role of altered load versus differential tissue response on the anatomical, cellular and molecular processes that contribute to the strength of such composite structures.
Abstract: Excessive, repetitive and altered loading have been implicated in the initiation of a series of soft- and hard-tissue responses or ;functional adaptations' of masticatory and locomotor elements. Such adaptive plasticity in tissue types appears designed to maintain a sufficient safety factor, and thus the integrity of given element or system, for a predominant loading environment(s). Employing a mammalian species for which considerable in vivo data on masticatory behaviors are available, genetically similar domestic white rabbits were raised on diets of different mechanical properties so as to develop an experimental model of joint function in a normal range of physiological loads. These integrative experiments are used to unravel the dynamic inter-relationships among mechanical loading, tissue adaptive plasticity, norms of reaction and performance in two cranial joint systems: the mandibular symphysis and temporomandibular joint (TMJ). Here, we argue that a critical component of current and future research on adaptive plasticity in the skull, and especially cranial joints, should employ a multifaceted characterization of a functional system, one that incorporates data on myriad tissues so as to evaluate the role of altered load versus differential tissue response on the anatomical, cellular and molecular processes that contribute to the strength of such composite structures. Our study also suggests that the short-term duration of earlier analyses of cranial joint tissues may offer a limited notion of the complex process of developmental plasticity, especially as it relates to the effects of long-term variation in mechanical loads, when a joint is increasingly characterized by adaptive and degradative changes in tissue structure and composition. Indeed, it is likely that a component of the adaptive increases in rabbit TMJ and symphyseal proportions and biomineralization represent a compensatory mechanism to cartilage degradation that serves to maintain the overall functional integrity of each joint system. Therefore, while variation in cranial joint anatomy and performance among sister taxa is, in part, an epiphenomenon of interspecific differences in diet-induced masticatory stresses characterizing the individual ontogenies of the members of a species, this behavioral signal may be increasingly mitigated in over-loaded and perhaps older organisms by the interplay between adaptive and degradative tissue responses.

Content maybe subject to copyright    Report

Citations
More filters
Book
01 Jan 2011
TL;DR: Hallgrimsson and Hall as mentioned in this paper discussed the link between phenotype and genotype in development and evolution, and proposed an approach to link phenotype and phenotype in the context of development, and discussed the developmental route to functional integration.
Abstract: Epigenetics: Linking Genotype and Phenotype in Development and Evolution 1. Introduction: Emergent Properties and the Phenotype Hallgrimsson and Hall Historical and Philosophical Foundations 2. Historical Foundations Brian K. Hall 3. Heuristic Reductionism and the Relative Significance of Inheritance James Grisemer Approaches to Epigenetics 4. Genomic imprinting Vett Lloyd 5. Methylation Mapping in Humans Christoph Grunau, Montpellier 6. Asexuality and Epigenetic Variation Root Gorelick, Manfred Laubichler and Rachel Massicotte 7. Preformation and the Humpty Dumpty Problem Ellie Larsen 8. A Principle of Developmental Inertia Allesandro Minelli Epigenetics of Vertebrate Organ Development 9. Nervous System Development Carol Schuurmans 10. Morphogenesis of pigment patterns Lennart Olsson 11. Interactions of the Cardiac Neural Crest Margaret Kirby 12. Bone and Cartilage Development Tamara Franz-Odendaal 13. Muscle-Bone Interactions and the Development of Skeletal Phenotype Sue Herring 14. Apical Ectoderm in the Developing Vertebrate Limb Cooper, L.N, Armfield, B.A., J.G.M. Thewissen 15. Role of Skeletal Muscle in the Shaping of Organs, Tissues and Cell Fate Choices Boris Kablar Epigenetics in Evolution and Disease 16. Integration, Complexity and Evolvability of the Head Dan Lieberman 17. Epigenetic interactions: The developmental route to functional integration Miriam Leah Zelditcha and Donald L. Swiderski 18. Epigenetic Contributions to Adaptive Radiation Susan Foster 19. Learning, Developmental Plasticity, and the Rate of Morphological Evolution Rich Palmer and Chris Neufeld 20. Epigenetics: Adaptation or Contingency Thomas Hansen 21. Dysmorphology Joan Richtsmeier 22. Human Disease Peter Gluckman 23. Epigenetics: The Context of Development Hallgrimsson and Hall

110 citations

Journal ArticleDOI
TL;DR: It is argued that better data are needed on the relationship between dietary categories, food material and geometric properties, the amount of time/cycles associated with different feeding behaviors, and mandible stress and strain patterns if the authors are to understand fully relationships between mandibular morphology and diet in primates.
Abstract: Attempts to establish relationships between mandibular morphology and either traditional dietary categories or geometric and material properties of primate diets have not been particularly successful. Using our conceptual framework of the feeding factors impacting mandibular morphology, we argue that this is because dietary categories and food geometric and material properties affect mandibular morphology only through intervening variables that are currently poorly understood, i.e., feeding behavior, mandibular loading, and stress and strain regimes. Our studies of 3-dimensional jaw kinematics in macaques and capuchins show that, although jaw movement profiles during chewing are affected by food material properties and species-level effects, patterns of jaw movements in these two species are broadly similar. However, because mandibular loading, stress, and strain regimes are determined by interactions between feeding behavior (such as jaw kinematics) and mandibular morphology, it is difficult to say whether these similarities in chewing kinematics also mean similarities in loading, stress, and strain. Comparative analyses of the scaling of daily feeding time and chew cycle duration reveal only weak support for the hypothesis that larger primates chew more than smaller primates. Consideration of these results suggests that better data are needed on the relationship between dietary categories, food material and geometric properties, the amount of time/cycles associated with different feeding behaviors (ingestion, premolar biting, mastication), and mandible stress and strain patterns if we are to understand fully relationships between mandibular morphology and diet in primates.

96 citations


Cites background from "Pushing the limit: masticatory stre..."

  • ...…mandibular mineralization, and cartilage and bone morphology, including wider and longer mandibular condyles, thicker mandibular corpora, deeper and wider symphyses, and thicker cortical bone at the symphysis (De Jong 2011; de Jong et al. 2010; Ravosa et al. 2007, 2010; Taylor et al. 2006)....

    [...]

Journal ArticleDOI
TL;DR: It is shown that hard-object feeding cannot explain the extreme morphology of Paranthropus boisei, and analysis of long-term dietary plasticity in an animal model suggests year-round reliance on tough foods requiring prolonged postcanine processing in P. boISEi.
Abstract: The robust jaws and large, thick-enameled molars of the Plio–Pleistocene hominins Australopithecus and Paranthropus have long been interpreted as adaptations for hard-object feeding. Recent studies of dental microwear indicate that only Paranthropus robustus regularly ate hard items, suggesting that the dentognathic anatomy of other australopiths reflects rare, seasonal exploitation of hard fallback foods. Here, we show that hard-object feeding cannot explain the extreme morphology of Paranthropus boisei. Rather, analysis of long-term dietary plasticity in an animal model suggests year-round reliance on tough foods requiring prolonged postcanine processing in P. boisei. Increased consumption of such items may have marked the earlier transition from Ardipithecus to Australopithecus, with routine hard-object feeding in P. robustus representing a novel behaviour.

83 citations

Journal ArticleDOI
TL;DR: Relationships among feeding system morphology, feeding behavior, and diet not only explain the morphological diversity of extant primates, but can also be used to reconstruct feeding behavior and diet in fossil taxa.
Abstract: Feeding is the set of behaviors whereby organisms acquire and process the energy required for survival and reproduction. Thus, feeding system morphology is presumably subject to selection to maintain or improve feeding performance. Relationships among feeding system morphology, feeding behavior, and diet not only explain the morphological diversity of extant primates, but can also be used to reconstruct feeding behavior and diet in fossil taxa. Dental morphology has long been known to reflect aspects of feeding behavior and diet but strong relationships of craniomandibular morphology to feeding behavior and diet have yet to be defined.

69 citations

Journal ArticleDOI
TL;DR: Analysis of three‐dimensional coordinate landmark data indicate that the basicrania of hard/tough diet rabbits exhibit more robust middle cranial fossae and pterygoid plates, as well as altered overall morphology of the caudal Cranial fossa, suggesting that long‐term variation in masticatory forces associated with differences in dietary properties can contribute to the complex and multifactorial development of neurocranial morphology.
Abstract: The evolutionary significance of cranial form and robusticity in early Homo has been variously attributed to allometry, encephalization, metabolic factors, locomotor activity, and masticatory forces. However, the influence of such factors is variably understood. To evaluate the effect of masticatory loading on neurocranial form, sibling groups of weanling white rabbits were divided into two cohorts of 10 individuals each and raised on either a soft diet or a hard/tough diet for 16 weeks until subadulthood. Micro-CT was used to quantify and visualize morphological variation between treatment groups. Results reveal trends (P < 0.10) for greater outer table thickness of the frontal bones, zygomatic height, and cranial globularity in rabbits raised on a hard/tough diet. Furthermore, analyses of three-dimensional coordinate landmark data indicate that the basicrania of hard/tough diet rabbits exhibit more robust middle cranial fossae and pterygoid plates, as well as altered overall morphology of the caudal cranial fossa. Thus, long term increases in masticatory loads may result in thickening of the bones of the neurocranial vault and/or altering the curvature of the walls. Differences in cranial regions not directly associated with the generation or resistance of masticatory forces (i.e., frontal bone, basicranium) may be indirectly correlated with diet-induced variation in maxillomandibular morphology. These findings also suggest that long-term variation in masticatory forces associated with differences in dietary properties can contribute to the complex and multifactorial development of neurocranial morphology.

67 citations

References
More filters
Book
01 Jan 2003

4,928 citations

ReportDOI
01 Jan 1995

2,339 citations


"Pushing the limit: masticatory stre..." refers methods in this paper

  • ...Using the NIST tabulation of mass attenuation coefficients (Hubbell and Selzer, 2001), the effective energy for Northwestern University’s Scanco MicroCT 40 operated at 70·kV is about 30·keV....

    [...]

Journal ArticleDOI
TL;DR: For thirty-two areas of cartilage from nine osteo-arthritic and four "normal" femoral heads a histologic-histochemical grade was assigned as an index of severity of the osteo -arthritic process.
Abstract: For thirty-two areas of cartilage from nine osteo-arthritic and four "normal" femoral heads a histologic-histochemical grade was assigned as an index of severity of the osteo-arthritic process. The DNA and hexosamine concentrations were determined as indicators of cell density and polysaccharide con

2,168 citations


"Pushing the limit: masticatory stre..." refers background in this paper

  • ...progressively deeper zones of TMJ articular cartilage are as follows: articular, filamentous network of elongate cells densely packed and tangentially arranged (high H2O, low proteoglycan, collagen rich); proliferative, ovoid or circular cells random in distribution (proteoglycan/protein production area); chondroblastic, large cell bundles arranged in columns (tidemark separates this from subjacent layer); hypertrophic chondrocyte/calcified, cells heavily encrusted in apatitic salts (Mankin et al., 1971; Newton and Nunamaker, 1985; Ostergaard et al., 1999)....

    [...]

  • ...Lower proteoglycan content throughout the FC pad and in the lower two layers of the condylar cartilage of O-diet rabbits mirrors findings for the articular surface of mammal limb elements, where age-related onset of cartilage degradation is linked to decreases in proteoglycan content (Mankin et al., 1971; Newton and Nunamaker, 1985; Haskin et al., 1995; Ostergaard et al., 1999)....

    [...]

  • ...…condylar cartilage of O-diet rabbits mirrors findings for the articular surface of mammal limb elements, where age-related onset of cartilage degradation is linked to decreases in proteoglycan content (Mankin et al., 1971; Newton and Nunamaker, 1985; Haskin et al., 1995; Ostergaard et al., 1999)....

    [...]

  • ...…(proteoglycan/protein production area); chondroblastic, large cell bundles arranged in columns (tidemark separates this from subjacent layer); hypertrophic chondrocyte/calcified, cells heavily encrusted in apatitic salts (Mankin et al., 1971; Newton and Nunamaker, 1985; Ostergaard et al., 1999)....

    [...]

  • ...…in cartilage composition reflect the early onset and progression of degenerative effects that compromise the structural integrity of a joint (Mankin et al., 1971; Newton and Nunamaker, 1985; Haskin et al., 1995; Kamelchuk and Major, 1995; Ishibashi et al., 1996; Ostergaard et al., 1999;…...

    [...]

Journal ArticleDOI
TL;DR: It is shown that VEGF-mediated capillary invasion is an essential signal that regulates growth plate morphogenesis and triggers cartilage remodeling and VEGf is anessential coordinator of chondrocyte death, chondROclast function, extracellular matrix remodeling, angiogenesis and bone formation in the growth plate.
Abstract: Hypertrophic chondrocytes in the epiphyseal growth plate express the angiogenic protein vascular endothelial growth factor (VEGF). To determine the role of VEGF in endochondral bone formation, we inactivated this factor through the systemic administration of a soluble receptor chimeric protein (Flt-(1-3)-IgG) to 24-day-old mice. Blood vessel invasion was almost completely suppressed, concomitant with impaired trabecular bone formation and expansion of hypertrophic chondrocyte zone. Recruitment and/or differentiation of chondroclasts, which express gelatinase B/matrix metalloproteinase-9, and resorption of terminal chondrocytes decreased. Although proliferation, differentiation and maturation of chondrocytes were apparently normal, resorption was inhibited. Cessation of the anti-VEGF treatment was followed by capillary invasion, restoration of bone growth, resorption of the hypertrophic cartilage and normalization of the growth plate architecture. These findings indicate that VEGF-mediated capillary invasion is an essential signal that regulates growth plate morphogenesis and triggers cartilage remodeling. Thus, VEGF is an essential coordinator of chondrocyte death, chondroclast function, extracellular matrix remodeling, angiogenesis and bone formation in the growth plate.

2,003 citations


"Pushing the limit: masticatory stre..." refers background in this paper

  • ...In the growth plate of a joint, apoptosis is a normal terminal event for hypertrophic chondrocytes, and such cells express angiogenic factors initiating vascular invasion, erosion of mineralized cartilage and bone formation (Gerber et al., 1999)....

    [...]

Journal ArticleDOI
12 Oct 2001-Science
TL;DR: Phenotypic responses in species interactions represent modifications that can lead to reciprocal change in ecological time, altered community patterns, and expanded evolutionary potential of species.
Abstract: When individuals of two species interact, they can adjust their phenotypes in response to their respective partner, be they antagonists or mutualists. The reciprocal phenotypic change between individuals of interacting species can reflect an evolutionary response to spatial and temporal variation in species interactions and ecologically result in the structuring of food chains. The evolution of adaptive phenotypic plasticity has led to the success of organisms in novel habitats, and potentially contributes to genetic differentiation and speciation. Taken together, phenotypic responses in species interactions represent modifications that can lead to reciprocal change in ecological time, altered community patterns, and expanded evolutionary potential of species.

1,485 citations


"Pushing the limit: masticatory stre..." refers background in this paper

  • ...628 Introduction Of late, adaptive plasticity has attracted considerable attention in myriad fields of biology (Gotthard and Nylin, 1995; Agrawal, 2001; Holden and Vogel, 2002; West-Eberhard, 2003)....

    [...]