Linking shape conspicuous asymmetry with shape covariation patterns and performance in the insect head and mandibles.

Bilateral symmetry is widespread across animals, yet, among bilaterians, many cases of conspicuous asymmetries evolved. This means that bilaterally homologous structures on the left and right side display divergent phenotypes. Evolution of such divergent phenotypes between otherwise similarly shaped structures can be thought to be favoured by modularity, but this has rarely been studied in the context of left-right differences. Here, we provide an empirical example, using geometric morphometrics, to assess patterns of asymmetry and covariation between landmark partitions in a grasshopper with conspicuously asymmetric mandibles. Our morphometric data confirms the presence of strictly directional conspicuous asymmetry in the mandibles, and surrounding structures. Covariance patterns and tests hint at a strong integration between mandibles despite their divergent morphologies, and variational modularity with the head capsule. While mandibles have been selected to achieve a key-and-lock morphology by having interlocking shapes, the developmental modularity required to achieve this seems to be overwritten by developmental and/or functional integration, allowing the precise matching required for feeding. The consequent conflicting covariation patterns are reminiscent of the palimpsest model. Finally, the degree of directional asymmetry appears to be under selection, although we find no relationship between bite force and mandible shape or asymmetry.

A comparison of dissection and 3D approaches to estimate muscle physiological cross-sectional area, validated by in vivo bite forces.

Performance traits such as bite forces are crucial to fitness and relate to the niche and adaptation of species. However, for many insects it is not possible to directly measure bite forces because they are too small. Biomechanical models of bite forces are therefore relevant to test hypotheses of adaptation in insects and other small organisms. Although such models are based on classical mechanics, combining forces, material properties and laws of levers, it is currently unknown how various models relate to bite forces measured in vivo. One critical component of these models is the physiological cross-sectional area (PCSA) of muscles, which relates to the maximum amount of force they can produce. Here, using the grasshopper Schistocerca gregaria, we compare various ways to obtain PCSA values and use in vivo measurements of bite forces to validate the biomechanical models. We show that most approaches used to derive PCSA (dissection, 3D muscle convex hull volume, muscle attachment area) are consistent with the expected relationships between PCSA and bite force, as well as with the muscle stress values known for insects. The only exception to this are PCSA values estimated by direct 3D muscle volume computation, which could be explained by noisy variation produced by shrinkage. This method therefore produces PCSA values which are uncorrelated to in vivo bite forces. Furthermore, despite the fact that all other methods do not significantly differ from expectations, their derived PCSA values vary widely, suggesting a lack of comparability between studies relying on different methods.

Morphometric models for estimating bite force in Mus and Rattus: mandible shape and size perform better than lever-arm ratios.

Morphological traits are frequently used as proxies for functional outputs such as bite force performance. This allows researchers to infer and interpret the impacts of functional variation, notably in adaptive terms. Despite their mechanical bases, the predictive power of these proxies for performance is not always tested. In particular, their accuracy at the intraspecific level is rarely assessed, and they have sometimes been shown to be unreliable. Here, we compared the performance of several morphological proxies in estimating in vivo bite force, across five species of murine rodents, at the interspecific and intraspecific levels. Proxies used included the size and shape of the mandible, as well as individual and combined muscular mechanical advantage (temporalis, superficial masseter and deep masseter). Maximum voluntary bite force was measured in all individuals included. To test the accuracy of predictions allowed by the proxies, we combined linear regressions with a leave-one-out approach, estimating an individual's bite force based on the rest of the dataset. The correlations between estimated values and the in vivo measurements were tested. At the interspecific and intraspecific levels, size and shape were better estimators than mechanical advantage. Mechanical advantage showed some predictive power at the interspecific level, but generally not within species, except for the deep masseter in Rattus In a few species, size and shape did not allow us to predict bite force. Extrapolations of performance based on mechanical advantage should therefore be used with care, and are mostly unjustified within species. In the latter case, size and shape are preferable.

One skull to rule them all? Descriptive and comparative anatomy of the masticatory apparatus in five mouse species.

Murine rodents display a unique cranial morphology and masticatory musculature. Yet detailed myological descriptions are scarce, especially considering the great diversity of the subfamily and the use of the house mouse and brown rat as model organisms. The masticatory musculature in these two species has been thoroughly described, which allows comparisons with other wild species. Description and comparison of a wide range of species constitutes a necessary step to fully understand how ecological factors may influence the morphology and myology of the skull in the Murinae and vice versa. In this study, we describe the masticatory musculature of five mouse species: Mus caroli, Mus cervicolor, Mus pahari, Mus fragilicauda, and Mus minutoides. For each species, one to five specimens were dissected, and their muscle weights and volumes calculated. One specimen was selected for iodine-enhanced CT-scanning, which allowed us to digitally reconstruct the musculature. We then compared the different masticatory arrangements between these species, as well as with the previous descriptions of the house mouse and brown rat. We show that interspecific differences especially involved the temporalis muscle and zygomatico-mandibularis muscular groups, although some differences were also seen in the pterygoid muscle and masseter muscle groups. We then propose some ecological interpretations for these differences, by interpreting them in terms of functional differences.

Skull Size and Biomechanics are Good Estimators of In Vivo Bite Force in Murid Rodents.

Rodentia is a species-rich group with diversified modes of life and diets. Although rodent skull morphology has been the focus of a voluminous literature, the functional significance of its variations has yet to be explored in live animals. Myomorphous rodents, including murids, have been suggested to represent "high-performance generalists." We measured in vivo bite force in 14 species of wild and lab-reared murid rodents of various sizes and diets to investigate potential morphofunctional differences between them. We dissected their skulls and computed a biomechanical model to estimate bite force. We first tested if our model allowed good estimation of in vivo data. Then, using morphological, in vivo and estimated bite force data in a phylogenetic context, we aimed to find the drivers of bite force differences among species. Estimated and in vivo bite forces were strongly correlated, which indicates that (a) biomechanical models allow a good estimation of real performance, and that (b) size and muscular changes (increased mass, fiber length, and PCSA) are the main drivers of bite performance differences. Myomorphous rodents, therefore, may have evolved high bite force through a combination of changes in size and musculature, which gave them a great versatility in their ability to process food. We found mixed results at the intraspecific level, with only some species displaying a good fit between estimated and in vivo measurements. We suggest that limited variation in size and muscular organization, and increased behavioral variation might decrease the precision of bite force estimates within species. Anat Rec, 301:256-266, 2018. © 2018 Wiley Periodicals, Inc.

Sex reversal induces size and performance differences among females of the African pygmy mouse, Mus minutoides.

Differences in biological performance, at both intra- and inter-specific levels, have often been linked to morphology but seldom to behavioural or genotypic effects. We tested performance at the intraspecific level by measuring bite force in the African pygmy mouse, Mus minutoides. This species displays an unusual sex determination system, with sex-reversed, X*Y females carrying a feminizing X* chromosome. X*Y females cannot be differentiated from XX females based on external or gonadal morphology; however, they are known to be more aggressive. We found that bite force was higher in X*Y females than in other females and males. We then performed geometric morphometric analyses on their skulls and mandibles and found that the higher performance of X*Y females was mainly explained by a greater overall skull size. The effects of the X* chromosome thus go beyond feminization, and extend to whole-organism performance and morphology. Our results also suggest limited effects of behaviour on bite force.

Ecomorphological analysis of the astragalo-calcaneal complex in rodents and inferences of locomotor behaviours in extinct rodent species.

Studies linking postcranial morphology with locomotion in mammals are common. However, such studies are mostly restricted to caviomorphs in rodents. We present here data from various families, belonging to the three main groups of rodents (Sciuroidea, Myodonta, and Ctenohystrica). The aim of this study is to define morphological indicators for the astragalus and calcaneus, which allow for inferences to be made about the locomotor behaviours in rodents. Several specimens were dissected and described to bridge the myology of the leg with the morphology of the bones of interest. Osteological characters were described, compared, mechanically interpreted, and correlated with a "functional sequence" comprising six categories linked to the lifestyle and locomotion (jumping, cursorial, generalist, fossorial, climber and semi-aquatic). Some character states are typical of some of these categories, especially arboreal climbers, fossorial and "cursorial-jumping" taxa. Such reliable characters might be used to infer locomotor behaviours in extinct species. Linear discriminant analyses (LDAs) were used on a wider sample of species and show that astragalar and calcaneal characters can be used to discriminate the categories among extant species whereas a posteriori inferences on extinct species should be examined with caution.