Evolutionary biomechanics: hard tissues and soft evidence?

Abstract

Biomechanical modelling is a powerful tool for quantifying the evolution of functional performance in extinct animals to understand key anatomical innovations and selective pressures driving major evolutionary radiations. However, the fossil record is composed predominantly of hard parts, forcing palaeontologists to reconstruct soft tissue properties in such models. Rarely are these reconstruction approaches validated on extant animals, despite soft tissue properties being highly determinant of functional performance. The extent to which soft tissue reconstructions and biomechanical models accurately predict quantitative or even qualitative patterns in macroevolutionary studies is therefore unknown. Here, we modelled the masticatory system in extant rodents to objectively test the ability of current muscle reconstruction methods to correctly identify quantitative and qualitative differences between macroevolutionary morphotypes. Baseline models generated using measured soft tissue properties yielded differences in muscle proportions, bite force, and bone stress expected between extant sciuromorph, myomorph, and hystricomorph rodents. However, predictions from models generated using reconstruction methods typically used in fossil studies varied widely from high levels of quantitative accuracy to a failure to correctly capture even relative differences between macroevolutionary morphotypes. Our novel experiment emphasizes that correctly reconstructing even qualitative differences between taxa in a macroevolutionary radiation is challenging using current methods. Future studies of fossil taxa should incorporate systematic assessments of reconstruction error into their hypothesis testing and, moreover, seek to expand primary datasets on muscle properties in extant taxa to better inform soft tissue reconstructions in macroevolutionary studies.

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

“…All other muscle AAs were not loaded, again to reflect the aggregation of muscle forces in the dry skull method. All other parameters remained unaltered from the 'extant iteration' of models presented in Broyde et al [36].…”

“…recovered in these same three rodent specimens using muscle volume sculpture reconstruction. Using volume sculpture, one investigator recovered 29% accuracy in the relative ordering of muscle PCSA in these rodents, while two other investigators independently yielded 63% and 75% accuracy [36]. Sensitivity or parameter-specific error tests are relatively commonplace in both MDA and FE modelling studies (e.g.…”

“…By contrast, guinea pigs (hystricomorph) have relatively low overall muscle mass for their skull size, but also possess a more robust morphology of the zygomatic arch leading to lower stresses [36,46,47] (figure 3d). The failure to capture these qualitative adaptive differences, and indeed, the relatively poor performance of the MAA-based models overall, is a stark contrast to the accuracy of the volume sculpture model iterations presented by Broyde et al [36], where the majority of models produced qualitatively accurate stress predictions and some iterations yielded extremely accurate quantitative predictions (figure 3c; electronic supplementary material, figure S8). Indeed, even the worst qualitatively performing volume sculpture model out-performs the MAA-based models presented here (figure 3c; electronic supplementary material, figure S8).…”

“…These models, built using muscle parameters measured in the same specimens being modelled, are referred to here as the ‘extant model’ iterations, as in Broyde et al . [ 36 ].…”

“…In this study, we extend a recently published examination of soft tissue reconstruction and biomechanical modelling in macroevolutionary studies [ 36 ] to MAA-based approaches to assess quantitatively the capacity of these methods to correctly predict established differences between macroevolutionary morphotypes. This not only allows us to assess the qualitative and quantitative accuracy of MAA-based approaches, but also enables comparisons with alternative volumetric sculpture methods widely used in palaeontological studies (e.g.…”