Joint Loads in Marsupial Ankles Reflect Habitual Bipedalism versus Quadrupedalism

Abstract

Joint surfaces of limb bones are loaded in compression by reaction forces generated from body weight and musculotendon complexes bridging them. In general, joints of eutherian mammals have regions of high radiodensity subchondral bone that are better at resisting compressive forces than low radiodensity subchondral bone. Identifying similar form-function relationships between subchondral radiodensity distribution and joint load distribution within the marsupial postcranium, in addition to providing a richer understanding of marsupial functional morphology, can serve as a phylogenetic control in evaluating analogous relationships within eutherian mammals. Where commonalities are established across phylogenetic borders, unifying principles in mammalian physiology, morphology, and behavior can be identified. Here, we assess subchondral radiodensity patterns in distal tibiae of several marsupial taxa characterized by different habitual activities (e.g., locomotion). Computed tomography scanning, maximum intensity projection maps, and pixel counting were used to quantify radiodensity in 41 distal tibiae of bipedal (5 species), arboreal quadrupedal (4 species), and terrestrial quadrupedal (5 species) marsupials. Bipeds (Macropus and Wallabia) exhibit more expansive areas of high radiodensity in the distal tibia than arboreal (Dendrolagus, Phascolarctos, and Trichosurus) or terrestrial quadrupeds (Sarcophilus, Thylacinus, Lasiorhinus, and Vombatus), which may reflect the former carrying body weight only through the hind limbs. Arboreal quadrupeds exhibit smallest areas of high radiodensity, though they differ non-significantly from terrestrial quadrupeds. This could indicate slightly more compliant gaits by arboreal quadrupeds compared to terrestrial quadrupeds. The observed radiodensity patterns in marsupial tibiae, though their statistical differences disappear when controlling for phylogeny, corroborate previously documented patterns in primates and xenarthrans, potentially reflecting inferred limb use during habitual activities such as locomotion. Despite the complex nature of factors contributing to joint loads, broad observance of these patterns across joints and across a variety of taxa suggests that subchondral radiodensity can be used as a unifying form-function principle within Mammalia.

Trabecular and cortical bone structure of the talus and distal tibia in Pan and Homo

“…As these individual trabeculae appear able to adapt to accommodate regional strains, it is likely that regional architectural parameters can provide information about how different areas of a joint are loaded. For example, trabecular and cortical bone distribution close to the articular surface, radiodensity patterns, and indicators of bone remodeling, correspond with predicted locations of peak loading associated with specific joint positions (Carlson, Jashashvili, Houghton, Westaway, & Patel, ; Mazurier, Nakatsukasa, & Macchiarelli, ; Patel & Carlson, ; Polk, Blumenfeld, & Ahluwalia, ; Polk, Williams, Peterson, Roseman, & Godfrey, ; Skinner et al, ; Tsegai et al, ; Zeininger, Richmond, & Hartman, ).…”

“…At the distal tibia, the orientation of trabecular bone in humans and chimpanzees corresponds with measurements of dorsiflexion at the ankle (Barak, Lieberman, Raichlen et al, 2013). Previous studies have assessed cortical thickness and radiodensity patterns of the articular surfaces of the primate talus and distal tibia (talus: Su, ; tibia: Carlson et al, ; Su, ), and behavioral correlates have been identified from bone profiles and radiodensity patterns at articular surfaces of other primate and mammalian taxa and epiphyses (Carlson et al, ; Mazurier et al, ; Patel & Carlson, ). However, to our knowledge no previous study has comparatively analyzed cortical thickness maps in both the talus and distal tibia of humans and chimpanzees.…”

Trabecular architecture in the StW 352 fossil hominin calcaneus

“…While subchondral bone apparent density patterns have proven useful in documenting the loading history of joints in extant animals (Carlson and Patel, 2006;Carlson, 2007, 2008;Polk et al, 2008;Nowak et al, 2010;Su, 2011;Carlson et al, 2013), there are obstacles in applying this approach to fossils. Namely, local variation in diagenetic processes can differentially affect mineralization of a joint region.…”

Spatial Subchondral Bone Density Reflecting Joint Loading of the Talus in Different Canidae

“…The functional anatomy of joints can be used to study joint biomechanics and to reveal differences in gait and limb use in specific species. 5,29,34 Studies on the evolutionary aspect of locomotion have used the general form-function relationship as the central mechanism in bone biology. 34 Gross differences have been described between bipedal and quadrupedal primates 29 and between arboreal and terrestrial marsupials.…”