The shrew tamed by Wolff's law: do functional constraints shape the skull through muscle and bone covariation?

Abstract

Bone is a highly plastic tissue that reflects the many potential sources of variation in shape. Here, we focus on the functional aspects of bone remodeling. We choose the skull for our analyses because it is a highly integrated system that plays a fundamental role in feeding and is thus, likely under strong natural selection. Its principal mechanical components are the bones and muscles that jointly produce bite force and jaw motion. Understanding the covariations among these three components is of interest to understand the processes driving the evolution of the feeding apparatus. In this study, we quantitatively and qualitatively compare interactions between these three components in shrews from populations known to differ in shape and bite force. Bite force was measured in the field using a force transducer and skull shape was quantified using surface geometric morphometric approaches based on µCT-scans of the skulls of same individuals. The masseter, temporalis, pterygoideus, and digastricus muscles of these individuals were dissected and their cross sectional areas determined. Our results show strong correlations between bite force and muscle cross sectional areas as well as between bite force and skull shape. Moreover, bite force explains an important amount of skull shape variation. We conclude that interactions between bone shape and muscle characteristics can produce different morpho-functional patterns that may differ between populations and may provide a suitable target for selection to act upon.