Size And Locomotor Ecology Have Differing Effects on the External and Internal Morphologies of Squirrel (Rodentia: Sciuridae) Limb Bones

Abstract

Mammals exhibit a diverse range of limb morphologies that are associated with different locomotor ecologies and structural mechanics. Much remains to be investigated, however, about the combined effects of locomotor modes and scaling on the external shape and structural properties of limb bones. Here, we used squirrels (Sciuridae) as a model clade to examine the effects of locomotor mode and scaling on the external shape and structure of the two major limb bones, the humerus and femur. We quantified humeral and femoral morphologies using 3D geometric morphometrics and bone structure analyses on a sample of 76 squirrel species across their four major ecotypes. We then used phylogenetic generalized linear models to test how locomotor ecology, size, and their interaction influenced morphological traits. We found that size and locomotor mode exhibit different relationships with the external shape and structure of the limb bones, and that these relationships differ between the humerus and femur. External shapes of the humerus and, to a lesser extent, the femur are best explained by locomotor ecology rather than by size, whereas structures of both bones are best explained by interactions between locomotor ecology and scaling. Interestingly, the statistical relationships between limb morphologies and ecotype were lost when accounting for phylogenetic relationships among species under Brownian motion. That assuming Brownian motion confounded these relationships is not surprising considering squirrel ecotypes are phylogenetically clustered; our results suggest that humeral and femoral variation partitioned early between clades and their ecomorphologies were maintained to the present. Overall, our results show how mechanical constraints, locomotor ecology, and evolutionary history may enact different pressures on the shape and structure of limb bones in mammals.

The carnivoran adaptive landscape reveals functional trade-offs among the skull, appendicular, and axial skeleton

“…In the appendicular skeleton, we confirmed hypotheses that the gradient from gracility to robustness often found as the primary source of variation across limb bone morphospace [40,41,55–59] signifies a functional trade-off between increasing cost of transport associated with cursoriality and resisting stresses associated with locomoting through resistant media (Fig. 2B).…”

“…It is well documented that adaptations in the elbows and knees facilitate the ability to generate large power strokes for turning and stabilizing the body while swimming [39,58,72,73]. These similar adaptations also enable semi-fossorial species to generate large forces to dig [39,59,67,69–71] and improve stability and load transfer during clearing [59,67,73,86]. What remains largely undetermined is the importance of increased axial joint rotation during swimming or digging.…”

“…HEI estimates the relative area of the distal end of the humerus available for the origins of the forearm flexors, pronators, and supinators. Ecomorphological studies suggest that increased HEI tends to be associated with increased fossorial behaviors by helping generate power, force, and stability [4,5,24,27–31]. However, the relationship between HEI and sizes of the forearm flexors, pronators, and supinators remains largely untested.…”

“…These similar adaptations also enable semi-fossorial species to generate large forces to dig [39,57,65,[67][68][69] and improve stability and load transfer during clearing [57,65,71,84]. What remains largely undetermined is the importance of increased axial joint rotation during swimming or digging.…”

Uncovering the mosaic evolution of the carnivoran skeletal system

“…In mammals, morphological innovations in the skull, appendicular skeleton and vertebral column facilitate the incredible diversity found today, ranging from bats with winged forelimbs to the biggest animals to have ever lived on Earth. Many researchers have examined how variation in the skull [1][2][3][4][5][6][7], limbs [8][9][10][11] or vertebrae [12][13][14][15][16] serve as crucial adaptations to their evolution. These skeletal systems are traditionally examined independently and are rarely investigated simultaneously even though these anatomical regions comprise a single, functionally integrated system that serves as structural support for movement, locomotion, and other life functions.…”