Intracranial and hierarchical perspective on dietary plasticity in mammals
TL;DR: Varying osteogenic responses in masticatory elements suggest that physiological adaptation, and corresponding variation in skeletal performance, may reside differentially at one level of bony architecture, potentially affecting the accuracy of behavioral and in silico reconstructions.
About: This article is published in Zoology.The article was published on 2017-03-16. It has received 14 citations till now. The article focuses on the topics: Masticatory force.
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TL;DR: The results are inconsistent with hypotheses that skull shape variation within marsupial species reflects a constraint pattern, but support suggestions that individual plasticity can be an important determinant of within-species shape variation in marsupials with high masticatory stresses.
Abstract: Within-species skull shape variation of marsupial mammals is widely considered low and strongly size-dependent (allometric), possibly due to developmental constraints arising from the altricial birth of marsupials. However, species whose skulls are impacted by strong muscular stresses – particularly those produced through mastication of tough food items – may not display such intrinsic patterns very clearly because of the known plastic response of bone to muscle activity of the individual. In such cases, allometry may not dominate within-species shape variation, even if it is a driver of evolutionary shape divergence; ordination of shape in a geometric morphometric context through principal component analysis (PCA) should reveal main variation in areas under masticatory stress (incisor region/zygomatic arches/mandibular ramus); but this main variation should emerge from high individual variability and thus have low eigenvalues. We assessed the evidence for high individual variation through 3D geometric morphometric shape analysis of crania and mandibles of three species of grazing-specialized wombats, whose diet of tough grasses puts considerable strain on their masticatory system. As expected, we found little allometry and low Principal Component 1 (PC1) eigenvalues within crania and mandibles of all three species. Also as expected, the main variation was in the muzzle, zygomatic arches, and masticatory muscle attachments of the mandibular ramus. We then implemented a new test to ask if the landmark variation reflected on PC1 was reflected in individuals with opposite PC1 scores and with opposite shapes in Procrustes space. This showed that correspondence between individual and ordinated shape variation was limited, indicating high levels of individual variability in the masticatory apparatus. Our results are inconsistent with hypotheses that skull shape variation within marsupial species reflects a constraint pattern. Rather, they support suggestions that individual plasticity can be an important determinant of within-species shape variation in marsupials (and possibly other mammals) with high masticatory stresses, making it difficult to understand the degree to which intrinsic constraints act on shape variation at the within-species level. We conclude that studies that link micro- and macroevolutionary patterns of shape variation might benefit from a focus on species with low-impact mastication, such as carnivorous or frugivorous species.
22 citations
Cites background or result from "Intracranial and hierarchical persp..."
...This is consistent with finds that the zygomatic arch grows differentially upon the onset of feeding in two marsupial species [Virginia opossums and New Guinea quolls [39, 40];], and remodels under mechanical stress in mammals [26, 37, 41, 42]....
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...As expected for a skull shaped by masticatory biomechanics [29, 31, 32, 37], the heat plots of hypothetical PC1 shape extremes within species reveal strikingly uniform patterns of high landmark displacement in the zygomatic arches and rostra, also consistent with our hypothesis that these areas should vary most within species (in the mandible, displacement directions are not as uniform but still all occur in the muscle attachment sites)....
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TL;DR: The research presented here highlights the importance of more naturalistic models of mammalian feeding, and underscores the need for a better understanding of the processes of both morphological and behavioral maturation that follow weaning.
20 citations
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...…and Hylander, 1981, 1996; Beecher et al., 1983; Bouvier and Zimny, 1987; Bouvier, 1988; Yamada and Kimmel, 1991; Kiliaridis et al., 1996; Nicholson et al., 2006; Ravosa et al., 2007, 2008b, 2010; Menegaz et al., 2009, 2010; Scott et al., 2014a; Franks et al., 2016, 2017; Ravosa et al., 2016)....
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TL;DR: It is demonstrated that bony architecture of the mandibular condyle in rabbits responds to variation in mechanical loading during an organism's lifetime and has the potential to track dietary variation within and among species.
Abstract: Although there is considerable evidence that bone responds to the loading environment in which it develops, few analyses have examined phenotypic plasticity or bone functional adaptation in the masticatory apparatus. Prior work suggests that masticatory morphology is sensitive to differences in food mechanical properties during development; however, the importance of the timing/duration of loading and variation in naturalistic diets is less clear. Here, we examined microstructural and macrostructural differences in the mandibular condyle in four groups of white rabbits (Oryctolagus cuniculus) raised for a year on diets that varied in mechanical properties and timing of the introduction of mechanically challenging foods, simulating seasonal variation in diet. We employed sliding semilandmarks to locate multiple volumes of interest deep to the mandibular condyle articular surface, and compared bone volume fraction, trabecular thickness and spacing, and condylar size/shape among experimental groups. The results reveal a shared pattern of bony architecture across the articular surface of all treatment groups, while also demonstrating significant among-group differences. Rabbits raised on mechanically challenging diets have significantly increased bone volume fraction relative to controls fed a less challenging diet. The post-weaning timing of the introduction of mechanically challenging foods also influences architectural properties, suggesting that bone plasticity can extend well into adulthood and that bony responses to changes in loading may be rapid. These findings demonstrate that bony architecture of the mandibular condyle in rabbits responds to variation in mechanical loading during an organism's lifetime and has the potential to track dietary variation within and among species.
14 citations
Cites background from "Intracranial and hierarchical persp..."
...Another complicating aspect of analyses examining adaptive plasticity and bone functional adaptation is that different skeletal regions exhibit variation in their sensitivity and responses to mechanical loading (Rawlinson et al., 1995; Pitsillides et al., 1999; Hsieh et al., 2001; Judex et al., 2004; Hamrick et al., 2006; Ravosa et al., 2010b, 2016; Franks et al., 2017)....
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TL;DR: Mechanical tests document significant decreases in articular cartilage stiffness corresponding to patterns of extracellular matrix relative protein abundance in rabbits subjected to greater cyclical loading, which indicates that TMJs routinely subjected to higher masticatory stresses due to a challenging diet eventually develop postnatal decreases in the ability to counter compressive loads during postcanine biting and chewing.
9 citations
Cites background or result from "Intracranial and hierarchical persp..."
...…et al., 2010; Franks et al., 2016, 2017), a finding that appears linked to the reduced mechanosensitivity of bone that comprises non-masticatory elements involved in protecting special sense organs from traumatic loads (Rawlinson et al., 1995; Hylander and Johnson, 1997; Franks et al., 2017)....
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...This argument is consistent with the presence of site-specific variation in plasticity responses between skeletal tissues subjected to similar mechanical stimuli (Rawlinson et al., 1995; Hsieh et al., 2001; Hamrick et al., 2006; Ravosa et al., 2007, 2010b, 2016; Franks et al., 2016, 2017)....
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...…exhibit postweaning plasticity of masticatory soft and hard tissues in response to diet-induced variation in jaw-loading patterns (Taylor et al., 2006; Ravosa et al., 2007, 2008, 2010a, 2015, 2016; Menegaz et al., 2009, 2010; Jašarević et al., 2010; Scott et al, 2014a,b; Franks et al., 2016, 2017)....
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...non-masticatory elements involved in protecting special sense organs from traumatic loads (Rawlinson et al., 1995; Hylander and Johnson, 1997; Franks et al., 2017)....
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...It has been argued that this condition is related to the need to maintain sufficient safety factors for traumatic loads surrounding the brain and sense organs (Hylander and Johnson, 1997; Ravosa et al., 2010b; Franks et al., 2016, 2017)....
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Western University of Health Sciences1, Polish Academy of Sciences2, Chinese Academy of Sciences3, Center for Excellence in Education4, Russian Academy of Sciences5, University of Toronto6, American Museum of Natural History7, Vanderbilt University8, University of Notre Dame9, University of Liverpool10, University of Adelaide11, University of Texas Southwestern Medical Center12, Southern Methodist University13
TL;DR: A review of the status of relevant aspects of lagomorph biology can be found in this paper, where the authors show that lagomorphs are a strong system to study macro-and micro-scale patterns of morphological change within a clade that offers underappreciated levels of diversity.
Abstract: Due to their global distribution, invasive history, and unique characteristics, European rabbits are recognizable almost anywhere on our planet. Although they are members of a much larger group of living and extinct mammals (Mammalia, Lagomorpha [rabbits, hares, and pikas]), the group is often characterized by several well-known genera (e.g., Oryctolagus, Sylvilagus, Lepus, and Ochotona). This representation does not capture the extraordinary diversity of behavior and form found throughout the order. Model organisms are commonly used as exemplars for biological research, but there are a limited number of model clades or lineages that have been used to study evolutionary morphology in a more explicitly comparative way. We present this review paper to show that lagomorphs are a strong system to study macro- and micro-scale patterns of morphological change within a clade that offers underappreciated levels of diversity. To this end, we offer a summary of the status of relevant aspects of lagomorph biology.
8 citations
References
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TL;DR: It appears that functional load-bearing prevents a remodeling process that would otherwise lead to disuse osteoporosis, and a small exposure to, or the first effect of, a suitable dynamic strain regimen appears to be sufficient to prevent the negatively balanced remodeling that is responsible for disuse fractures.
Abstract: In studies on a functionally isolated avian-bone preparation to which external loads could be applied in vivo, we determined the following information. Removal of load-bearing resulted in substantial remodeling endosteally, intracortically, and, to a lesser extent, periosteally. Since the balance of this remodeling was negative, bone mass declined. It therefore appears that functional load-bearing prevents a remodeling process that would otherwise lead to disuse osteoporosis. Four consecutive cycles a day of an externally applied loading regimen that engendered physiological strain magnitudes but an altered strain distribution prevented remodeling and was thus associated with no change in bone mass. A small exposure to, or the first effect of, a suitable dynamic strain regimen appears to be sufficient to prevent the negatively balanced remodeling that is responsible for disuse osteoporosis. Thirty-six 0.5-hertz cycles per day of the same load regimen also prevented intracortical resorption but was associated with substantial periosteal and endosteal new-bone formation. Over a six-week period, bone-mineral content increased to between 133 and 143 per cent of the original value. Physiological levels of strain imposed with an abnormal strain distribution can produce an osteogenic stimulus that is capable of increasing bone mass. Neither the size nor the character of the bone changes that we observed were affected by any additional increase in the number of load cycles from thirty-six to 1800. Clinical Relevance: The results of this experiment must be considered in relation to the type and duration of the non-physiological loads that were imposed.(ABSTRACT TRUNCATED AT 250 WORDS)
1,550 citations
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
TL;DR: A knowledge of the mechanisms and developmental patterns underlying phenotypic variation is crucial to the understanding of important evolutionary phenomena, and some biologists are predicting an increasing focus on this variation leading to a Renaissance of the Phenotype.
Abstract: Variation, the fuel that feeds evolutionary change, originates at the levels of both the genotype and the phenotype. Genetically identical organisms reared under different conditions may display quite distinct characteristics. Until recently, the types and sources of such phenotypic variation have been given little consideration in evolutionary theory. But a knowledge of the mechanisms and developmental patterns underlying phenotypic variation is crucial to the understanding of important evolutionary phenomena. Therefore some biologists are predicting an increasing focus on this variation leading to a Renaissance of the Phenotype.
1,106 citations
TL;DR: Several mathematical equations can be derived that provide simple parametric models for bone adaptation, which continuously adjusts skeletal mass and architecture to changing mechanical environments.
873 citations