BONES AND BURROWING: MECHANOADAPTATION IN Peromyscus

Mechanoadaptation is the ability to adapt in-vivo to mechanical loads. Bones adapt to increased mechanical loading by increasing size and density; to decreased loading by resorbing bone to decrease density; and to altered loading by changing the internal structure or external morphology. Mechanoadaptation is distinct from evolutionary adaptation (response to selection through evolution), as it occurs throughout the lifetime of an individual animal. Bone remodeling that occurs in-vivo is not heritable in and of itself. However, the capacity for mechanoadaptation, and the mechanisms through which mechanical forces are transduced into cellular signals, are heritable, and are subject to selection.

I recently collaborated with Sandra Shefelbine (Northeastern University) on a National Science Foundation Integrative Organismal Systems grant to investigate the relative influence of mechanoadaptation and evolutionary adaptation in the mammalian skeleton. Our plan focuses on Peromyscus (Rodentia: Cricetidae; deer mouse) to examine skeletal adaptations in the fore and hind limbs related to burrowing behavior. Several species of Peromyscus build burrows in the wild, and these burrows vary in size an complexity across the clade. Pioneering work by Hopi Hoekstra and colleagues identified the genetic basis of burrowing in the clade, but so far, no one has investigated how skeletal morphology relates to genetic and behavioral traits.

Our plan examines the various influences on morphology through ontogeny and across biological scale, from gene expression with RNAseq, to trabecular bone morphology, cortical bone shape, whole-bone mechanical properties, and organismal ecology. We have published our first set of investigations on Peromyscus fore- and hindlimbs, in collaboration with student Lindsey Young (Northeastern University). This work showed that wild-caught specimens of digging Peromyscus (P. polionotus) have limb bones that are more resistant to bending stress than lab-reared specimens, indicating that the ability to burrow during development has a significant effect on the development of functional morphology in this group. Additionally, digging Peromyscus have more robust tibial morphology (both in cross-sectional properties and trabecular bone properties). We are planning to combine in-vivo experiments with measurements of museum specimens to understand how evolution and mechanoadaptation share responsibility for skeletal shape, and how we can use that information to uncover broader principles governing the functional morphology of the mammalian skeleton.

Publications

Young, L.A., Munro, E., Somanchi, P., Bemis, A., Smith, S.M., Shefellbine, S. "Analysis of bone structure in Peromyscus : Effects of burrowing behavior." In press (2024). The Anatomical Record.