Back to the bones: do muscle area assessment techniques predict functional evolution across a macroevolutionary radiation?

Measures of attachment or accommodation area on the skeleton are a popular means of rapidly generating estimates of muscle proportions and functional performance for use in large-scale macroevolutionary studies. Herein, we provide the first evaluation of the accuracy of these muscle area assessment (MAA) techniques for estimating muscle proportions, force outputs and bone loading in a comparative macroevolutionary context using the rodent masticatory system as a case study. We find that MAA approaches perform poorly, yielding large absolute errors in muscle properties, bite force and particularly bone stress. Perhaps more fundamentally, these methods regularly fail to correctly capture many qualitative differences between rodent morphotypes, particularly in stress patterns in finite-element models. Our findings cast doubts on the validity of these approaches as means to provide input data for biomechanical models applied to understand functional transitions in the fossil record, and perhaps even in taxon-rich statistical models that examine broad-scale macroevolutionary patterns. We suggest that future work should go back to the bones to test if correlations between attachment area and muscle size within homologous muscles across a large number of species yield strong predictive relationships that could be used to deliver more accurate predictions for macroevolutionary and functional studies.