How does bone microanatomy and musculature covary? An investigation in the forelimb of two species of martens (Martes foina, Martes martes)

Abstract

The long bones and associated musculature play a prominent role in the support and movement of the body and are expected to reflect the associated mechanical demands. But in addition to the functional response to adaptive changes, the conjoined effects of phylogenetic, structural and developmental constraints also shape the animal's body. In order to minimise the effect of the aforementioned constraints and to reveal the biomechanical adaptations in the musculoskeletal system to locomotor mode, we here study the forelimb of two closely related martens: the arboreal pine marten (Martes martes) and the more terrestrial stone marten (Martes foina), focusing on their forelimb muscle anatomy and long bone microanatomy; and, especially, on their covariation. To do so, we quantified muscle data and bone microanatomical parameters and created 3D and 2D maps of the cortical thickness distribution for the three long bones of the forelimb. We then analysed the covariation of muscle and bone data, both qualitatively and quantitatively. Our results reveal that speciesspecific muscular adaptations are not clearly reflected in the microanatomy of the bones. Yet, we observe a global thickening of the bone cortex in the radius and ulna of the more arboreal pine marten, as well a stronger flexor muscle inserting on its elbow.We attribute these differences to variation in their locomotor modes. Analyses of our 2D maps revealed a shift of cortical thickness distribution pattern linked to ontogeny, rather than species-specific patterns. We found that although intraspecific variation is not negligible, species distinction was possible when taking muscular and bone microanatomical data into consideration. Results of our covariation analyses suggest that the muscle-bone correlation is linked to ontogeny rather than to muscular strength at zones of insertion. Indeed, if we find a correlation between cortical thickness distribution and the strength of some muscles in the humerus, that is not the case for the others and in the radius and ulna. Cortical thickness distribution appears rather linked to bone contact zones and ligament insertions in the radius and ulna, and to some extent in the humerus. We conclude that inference on muscle from bone microanatomy is possible only for certain muscles in the humerus.

Estimation of the forces exerted on the limb long bones of a white rhinoceros (Ceratotherium simum) using musculoskeletal modelling and simulation

“…The large moment arm of the ulnaris lateralis for elbow extension was due to the great caudo‐distal development of the lateral epicondyle of the humerus in large rhinos (compare Figure 1d,e in Mallet et al., 2019 ; see also Figure 5a ). This particular anatomical feature is not observed in smaller rhinoceroses ( Dicerorhinus sumatrensis ), nor in other perissodactyls, bovids and even hippopotamuses or elephants (Bader et al., 2022 ; Barone, 1999 ; CE, personal observation; Maclaren et al., 2018 ). Accordingly, data in horses do not indicate very strong activation of the ulnaris lateralis during locomotion (Harrison et al., 2010 ).…”