Intracranial and hierarchical perspective on dietary plasticity in mammals.

The effect of dietary properties on craniofacial form has been the focus of numerous functional studies, with increasingly more work dedicated to the importance of phenotypic plasticity. As bone is a dynamic tissue, morphological variation related to differential loading is well established for many masticatory structures. However, the adaptive osteogenic response of several cranial sites across multiple levels of bony organization remains to be investigated. Here, rabbits were obtained at weaning and raised for 48 weeks until adulthood in order to address the naturalistic influence of altered loading on the long-term development of masticatory and non-masticatory elements. Longitudinal data from micro-computed tomography (µCT) scans were used to test the hypothesis that variation in cortical bone formation and biomineralization in masticatory structures is linked to increased stresses during oral processing of mechanically challenging foods. It was also hypothesized that similar parameters for neurocranial structures would be minimally affected by varying loads as this area is characterized by low strains during mastication and reduced hard-tissue mechanosensitivity. Hypotheses were supported regarding bone formation for maxillomandibular and neurocranial elements, though biomineralization trends of masticatory structures did not mirror macroscale findings. 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. Together, these findings underscore the complexity of bone adaptation and highlight functional and developmental variation in determinants of skull form.

Betwixt and Between: Intracranial Perspective on Zygomatic Arch Plasticity and Function in Mammals.

The zygomatic arch is morphologically complex, providing a key interface between the viscerocranium and neurocranium. It also serves as an attachment site for masticatory muscles, thereby linking it to the feeding apparatus. Though morphological variation related to differential loading is well known for many craniomandibular elements, the adaptive osteogenic response of the zygomatic arch remains to be investigated. Here, experimental data are presented that address the naturalistic influence of masticatory loading on the postweaning development of the zygoma and other cranial elements. Given the similarity of bone-strain levels among the zygoma and maxillomandibular elements, a rabbit and pig model were used to test the hypothesis that variation in cortical bone formation and biomineralization along the zygomatic arch and masticatory structures are linked to increased stresses. It was also hypothesized that neurocranial structures would be minimally affected by varying loads. Rabbits and pigs were raised for 48 weeks and 8 weeks, respectively. In both experimental models, CT analyses indicated that elevated masticatory loading did not induce differences in cortical bone thickness of the zygomatic arch, though biomineralization was positively affected. Hypotheses were supported regarding bone formation for maxillomandibular and neurocranial elements. Varying osteogenic responses in the arch suggests that skeletal adaptation, and corresponding variation in performance, may reside differentially at one level of bony architecture. Thus, it is possible that phenotypic diversity in the mammalian zygoma is due more singularly to natural selection (vs. plasticity). These findings underscore the complexity of the zygomatic arch and, more generally, determinants of skull form. Anat Rec, 299:1646-1660, 2016. © 2016 Wiley Periodicals, Inc.

Limitations of a morphological criterion of adaptive inference in the fossil record.

Experimental analyses directly inform how an anatomical feature or complex functions during an organism's lifetime, which serves to increase the efficacy of comparative studies of living and fossil taxa. In the mammalian skull, food material properties and feeding behaviour have a pronounced influence on the development of the masticatory apparatus. Diet-related variation in loading magnitude and frequency induce a cascade of changes at the gross, tissue, cellular, protein and genetic levels, with such modelling and remodelling maintaining the integrity of oral structures vis-à-vis routine masticatory stresses. Ongoing integrative research using rabbit and rat models of long-term masticatory plasticity offers unique insight into the limitations of functional interpretations of fossilised remains. Given the general restriction of the palaeontological record to bony elements, we argue that failure to account for the disparity in the hierarchical network of responses of hard versus soft tissues may overestimate the magnitude of the adaptive divergence that is inferred from phenotypic differences. Second, we note that the developmental onset and duration of a loading stimulus associated with a given feeding behaviour can impart large effects on patterns of intraspecific variation that can mirror differences observed among taxa. Indeed, plasticity data are relevant to understanding evolutionary transformations because rabbits raised on different diets exhibit levels of morphological disparity comparable to those found between closely related primate species that vary in diet. Lastly, pronounced variation in joint form, and even joint function, can also characterise adult conspecifics that differ solely in age. In sum, our analyses emphasise the importance of a multi-site and hierarchical approach to understanding determinants of morphological variation, one which incorporates critical data on performance.

Chewed out: an experimental link between food material properties and repetitive loading of the masticatory apparatus in mammals.

Using a model organism (rabbits) that resembles a number of mammalian herbivores in key aspects of its chewing behaviors, we examined how variation in dietary mechanical properties affects food breakdown during mastication. Such data have implications for understanding phenotypic variation in the mammalian feeding apparatus, particularly with respect to linking jaw form to diet-induced repetitive loading. Results indicate that chewing frequency (chews/s) is independent of food properties, whereas chewing investment (chews/g) and chewing duration(s), which are proportional to repetitive loading of the jaws, are positively related to food stiffness and toughness. In comparisons of displacement-limited and stress-limited fragmentation indices, which respectively characterize the intraoral breakdown of tough and stiff foods, increases in chewing investment and duration are linked solely to stiffness. This suggests that stiffer foods engender higher peak loads and increased cyclical loading. Our findings challenge conventional wisdom by demonstrating that toughness does not, by itself, underlie increases in cyclical loading and loading duration. Instead, tough foods may be associated with such jaw-loading patterns because they must be processed in greater volumes owing to their lower nutritive quality and for longer periods of time to increase oral exposure to salivary chemicals.

Teaching an old jaw new tricks: diet-induced plasticity in a model organism from weaning to adulthood.

Many organisms exhibit a decrease in the ability to modify their phenotypes in response to shifts in environmental conditions as they mature. Such age-dependent plasticity has important implications in a variety of evolutionary and ecological contexts, particularly with respect to understanding adaptive responses to heterogeneous environments. In this study, we used experimental diet manipulation to examine the life-history trajectory of plasticity in the feeding complex of a model organism, the white rabbit (Oryctolagus cuniculus). We demonstrate that, contrary to expectations derived from previous cross-sectional studies of skeletal plasticity, the jaws of weanlings and young adults exhibit similar increases in relative bone cross-sectional areas in response to the introduction of mechanically challenging foods into their diets. Furthermore, we present evidence that sensitivity to loading patterns persists well into adulthood in some regions of the masticatory apparatus in rabbits, indicating that there is an extended window of opportunity to respond to changes in dietary properties during an animal's life span. We conclude that certain aspects of the facial skeleton of rabbits, and perhaps mammals in general, are sensitive to environmental stimuli long after skeletal maturity is achieved, highlighting the importance of plasticity as a source of adaptive variation at later life-history stages.

Experimental perspective on fallback foods and dietary adaptations in early hominins.

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.