Muscle‐induced loading as an important source of variation in craniofacial skeletal shape

Abstract

The shape of the craniofacial skeleton is constantly changing through ontogeny, and reflects a balance between developmental patterning and mechanical-load induced remodeling. Muscles are a major contributor to producing the mechanical environment that is crucial for “normal” skull development. Here we use an F5 hybrid population of Lake Malawi cichlids to characterize the strength and types of associations between craniofacial bones and muscles. We focus on four bones/bone complexes, with different developmental origins, alongside four muscles with distinct functions. We used micro-computed tomography to extract 3D information on bones and muscles. 3D geometric morphometrics and volumetric measurements were used to characterize bone and muscle shape, respectively. Linear regressions were performed to test for associations between bone shape and muscle volume. We identified three types of associations between muscles and bones: weak, strong direct (i.e., muscles insert directly onto bone), and strong indirect (i.e., bone is influenced by muscles without a direct connection). In addition, we show that whereas the shape of some bones are relatively robust to muscle-induced mechanical stimulus, others appear to be highly sensitive to muscular input. Our results imply that the roles for muscular input on skeletal shape extend beyond specific points of origin or insertion, and hold significant potential to influence broader patterns of craniofacial geometry. Thus, changes in the loading environment, either as a normal course of ontogeny or if an organism is exposed to a novel environment, may have predicable effects on skeletal shape via near and far-ranging effects of muscular loading.

Ecomorphological divergence and habitat lability in the context of robust patterns of modularity in the cichlid feeding apparatus

“…Tropheops residing in more shallow habitats exhibited a more robust feeding apparatus, while those Tropheops members residing in deeper habitats exhibited a more slender and gracile feeding apparatus [ 38 ]. The specific differences in morphology are predicted to influence feeding performance and biomechanics [ 46 , 47 ], and include the area for muscle or ligament attachment sites (i.e., increased maxillary shank area for A1 attachment, increase pharyngeal jaw keel for pharyngohyoideus attachment), as well as the length of bony process that would have the effect of changing the mechanical advantage (i.e., the ascending arm of the mandible, the wings of the pharyngeal jaw). These data formalize and extend previously published trends (e.g., [ 28 , 30 ]), and suggest the existence of two general Tropheops ecomorphs within Lake Malawi.…”

Does phenotypic plasticity initiate developmental bias?

“…For pumpkinseed, these polymorphisms are known to occur repeatedly across several populations in Ontario, Canada, as well as in the Adirondacks of New York State, which respectively form two lineages (Weese, Ferguson, & Robinson, 2012). Indeed, much of the similarity in these responses could simply be due to similar patterns of biomechanical stress and a common developmental response that has evolved ancestrally (Conith, Lam, & Albertson, 2019). Further, similar changes in response to the same type of diet treatments are also observed in the orangespotted sunfish (Lepomis humilis; Hegrenes, 2001).…”

“…Such information could be used to examine the presence, persistence, and function of alleles and developmental interactions across taxonomic levels. Indeed, much of the similarity in these responses could simply be due to similar patterns of biomechanical stress and a common developmental response that has evolved ancestrally (Conith, Lam, & Albertson, ).…”

Morphological association between the muscles and bones in the craniofacial region

“…The term epigenetics encompasses the tissue-tissue interactions, such as the effect of the muscle on the bone during their development and maintenance periods. The biomechanical interaction between the muscle and bone has typically been investigated in three types of studies, i.e., analyses of the correlation between muscle volume and bone size [8][9][10][11], comparisons of skull shapes between mice feeding on hard and soft diets [12,13], and study of the effects of muscle atrophy on bone shapes [13,14]. As with the muscle-bone interaction in adults, the bone shape is associated with the muscle-induced loading during the embryonic development period.…”