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

Karl T Bates,Michael J Fagan,Sarah Broyde,Linjie Wang,Matthew Dempsey,Philip G Cox

doi:10.1098/rsif.2021.0324

Abstract

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.

Highlights

To assess the accuracy of muscle area assessment (MAA) approaches, we used the skeletal, multi-body dynamics analysis (MDA) and finite-element (FE) models of the grey squirrel (Sciurus carolinensis), brown rat (Rattus norvegicus) and domestic guinea pig (Cavia porcellus) presented by Broyde et al [36]. These taxa are representative of masticatory morphotypes within the Rodentia, and have evolved disparate masticatory musculature and bite mechanics [43,44,45,46,47]. Models of these taxa allowed us to measure the accuracy of MAA approaches for predicting muscle physiological cross-sectional area (PCSA), bite force and bone stress against model iterations that use muscle force-generating properties directly measured through dissection and imaging [46,47]
The AA method gave similar errors in homologous muscles across the three morphotypes: the superficial masseter PCSA was underestimated by 96–99.3% in the three morphotypes; error in the medial pterygoid ranged from −78.2% to −96.3%; and the PCSA of the posterior deep masseter was underestimated by 89% and 91.4% in the squirrel and rat
MAA-based approaches to estimate muscle size and forcegenerating capacity, and subsequently bone loading, have been widely applied to extinct and extant taxa to examine the functional consequences of changing morphology and macroevolutionary patterns in the locomotor, axial and masticatory systems of vertebrates (e.g. [1,2,3,4,5,6,7,8,9,10,11,12,13,14,15,16,17,18,19,20,21,22,23,24,25,26,27])

Summary

Introduction

Calculations of the force-generating capacity of muscles, based on measurements of muscle attachment sites and/or areas delineated by osteological structures, are widely used in macroevolutionary studies of functional morphology and biomechanics (e.g. [1,2,3,4,5,6,7,8,9,10,11,12,13,14,15,16,17,18,19,20,21,22,23,24,25,26,27]). In extant taxa, extrapolating muscle size and mechanical performance from existing bony specimens circumvents time-, labour- and skill-intensive physiological and biomechanical experiments on live animals and/or cadavers, making it feasible to analyse large sample sizes statistically and rapidly, and assess broad-scale macroevolutionary patterns The ability of MAA-based methods to accurately reconstruct qualitative and quantitative functional patterns in a macroevolutionary radiation has not been extensively tested. In addition to the limited assessment in explicit macroevolutionary contexts, to our knowledge, no study has addressed the absolute or relative inaccuracy that MAA-based methods yield in finite-element studies of bone stress/strain, despite widespread combined use of these approaches. The extent to which MAA reconstruction approaches accurately predict quantitative or even qualitative patterns in macroevolutionary studies is, poorly constrained

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Results

Conclusion