Adaptive plasticity in the mouse mandible

Abstract

Background: Plasticity, i.e. non-heritable morphological variation, enables organisms to modify the shape of their skeletal tissues in response to varying environmental stimuli. Plastic variation may also allow individuals to survive in the face of new environmental conditions, enabling the evolution of heritable adaptive traits. However, it is uncertain whether such a plastic response of morphology constitutes an evolutionary adaption itself. Here we investigate whether shape differences due to plastic bone remodelling have functionally advantageous biomechanical consequences in mouse mandibles. Shape characteristics of mandibles from two groups of inbred laboratory mice fed either rodent pellets or ground pellets mixed with jelly were assessed using geometric morphometrics and mechanical advantage measurements of jaw adductor musculature.

Results: Mandibles raised on diets with differing food consistency showed significant differences in shape, which in turn altered their biomechanical profile. Mice raised on a soft food diet show a reduction in mechanical advantage relative to mice of the same inbred strain raised on a typical hard food diet. Further, the soft food eaters showed lower levels of integration between jaw regions, particularly between the molar and angular region relative to hard food eaters.

Conclusions: Bone remodelling in mouse mandibles allows for significant shifts in biomechanical ability. Food consistency significantly influences this process in an adaptive direction, as mice raised on hard food develop jaws better suited to handle hard foods. This remodelling also affects the organisation of the mandible, as mice raised on soft food appear to be released from developmental constraints showing less overall integration than those raised on hard foods, but with a shift of integration towards the most solicited regions of the mandible facing such a food, namely the incisors. Our results illustrate how environmentally driven plasticity can lead to adaptive functional changes that increase biomechanical efficiency of food processing in the face of an increased solicitation. In contrast, decreased demand in terms of food processing seems to release developmental interactions between jaw parts involved in mastication, and may generate new patterns of co-variation, possibly opening new directions to subsequent selection. Overall, our results emphasize that mandible shape and integration evolved as parts of a complex system including mechanical loading food resource utilization and possibly foraging behaviour.

Figure 1

Data collected for the morphometric and mechanical analyses the left mandible as an example. A: Morphometric data based on 15 landmarks and 45 semi landmarks sampled over 7 curves. The shaded regions indicate the 5 hypothesized developmental and functional modules [13,25]. B: The two inlever lengths (based on the temporal and masseter muscle insertions) and the two outlever lengths (based on bite points at the incisors and molars). These are used in various combinations to measure four distinct mechanical advantages (Temporal-Incisor, Temporal-Molar, Masseter-Incisor, Masseter-Molar). All scale bars = 3 mm.

Figure 2

Results of the mechanical analysis of mandible of mice reared on diets of different consistencies. The animals fed a hard food diet show higher residual values (equivalent here to higher mechanical advantages) than the mice fed on soft food. This holds for all four mechanical advantage measures, although the difference is more pronounced when the masseter is used.

Figure 3

Landmark-based analysis of the mandible shape of hard vs. soft food eaters. A. Morphological variation in the space of the first and third principal components of the mandible shape analysis. Hard food eaters: blue diamonds; soft food eaters: red circles. B and C. Visualization of the deformation associated with the two axes. Deformation has been magnified by taking extreme values along the axes: −0.1 (in blue)/+0.1 (in red). B. Deformation along PC1. C. Deformation along PC3.