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

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.

Functional morphology of the hindlimb of fossilized pygmy hippopotamus from Ayia Napa (Cyprus)

“…Often, prominent muscle attachment sites on bones are linked to powerful muscles (Etienne et al, 2021a; Houtekamer & Sondaar, 1979; Martin et al, 2019; Toledo et al, 2015). However, there are other studies arguing that the assessment of a strong muscle based on the development of its insertion area is not well supported (Bates et al, 2021; Bello‐Hellegouarch et al, 2013). It is, therefore, not completely certain whether the developed attachment areas of the bony elements of P. minor may have corresponded to powerful muscles.…”

Three-dimensional polygonal muscle modelling and line of action estimation in living and extinct taxa

“…The centroids of the attachment areas can either be estimated for extinct taxa 44 , 50 , 51 , 53 , 60 , 97 , 122 – 124 or measured/inferred from digitized attachment areas of extant taxa 69 , 73 , 74 , 78 , 79 , 88 , 125 . Additionally, we developed a code (Supplementary Information) to streamline musculoskeletal modelling workflows that now allows to directly calculate the attachment centroids and the attachment area for extinct and extant taxa from the vertices placed on the attachment area during the iterative polygonal muscle modelling approach presented herein (see Supplementary Information for muscle attachment definition) or for selected faces of a segmented muscle (i.e., diceCT or MRI) or selected faces of a muscle scar/attachment area on a bone, as follows.…”

“… 33 , 56 , 58 , 66 ), we present an approach similar to ‘box modelling’ 67 . In contrast to lofting a surface over multiple rings or curves (e.g., see 33 , 58 , 60 , 64 , 68 , 69 ) with only limited control, polygonal modelling allows adjustment of every vertex individually, to extrude new faces, as well as to create holes, which can later be filled (i.e., closed) again, allowing modelling of muscles with complex geometry (e.g., with multiple heads or tendons; see Supplementary Information). This new approach makes it possible to build the musculature in relatively low resolution and, therefore, permits quick adjustments.…”

A toolbox for the retrodeformation and muscle reconstruction of fossil specimens in Blender

“…Sellers et al [ 22 ], Wilken et al [ 23 ], Cost et al [ 19 ]) takes into account both origin and attachment areas, as well as muscle length. Bates et al [ 31 ] compared the Thomason [ 17 ] dry skull method and an approach based on attachment areas and found that for both methods, muscle properties, bite force, bone stress and stress patterns were less accurate compared to data and models obtained from cadaver data.…”