Trabecular architecture in the sciuromorph femoral head: allometry and functional adaptation

Abstract

BackgroundSciuromorpha (squirrels and close relatives) are diverse in terms of body size and locomotor behavior. Individual species are specialized to perform climbing, gliding or digging behavior, the latter being the result of multiple independent evolutionary acquisitions. Each lifestyle involves characteristic loading patterns acting on the bones of sciuromorphs. Trabecular bone, as part of the bone inner structure, adapts to such loading patterns. This network of thin bony struts is subject to bone modeling, and therefore reflects habitual loading throughout lifetime. The present study investigates the effect of body size and lifestyle on trabecular structure in Sciuromorpha.MethodsBased upon high-resolution computed tomography scans, the femoral head 3D inner microstructure of 69 sciuromorph species was analyzed. Species were assigned to one of the following lifestyle categories: arboreal, aerial, fossorial and semifossorial. A cubic volume of interest was selected in the center of each femoral head and analyzed by extraction of various parameters that characterize trabecular architecture (degree of anisotropy, bone volume fraction, connectivity density, trabecular thickness, trabecular separation, bone surface density and main trabecular orientation). Our analysis included evaluation of the allometric signals and lifestyle-related adaptation in the trabecular parameters.ResultsWe show that bone surface density, bone volume fraction, and connectivity density are subject to positive allometry, and degree of anisotropy, trabecular thickness, and trabecular separation to negative allometry. The parameters connectivity density, bone surface density, trabecular thickness, and trabecular separation show functional signals which are related to locomotor behavior. Aerial species are distinguished from fossorial ones by a higher trabecular thickness, lower connectivity density and lower bone surface density. Arboreal species are distinguished from semifossorial ones by a higher trabecular separation.ConclusionThis study on sciuromorph trabeculae supplements the few non-primate studies on lifestyle-related functional adaptation of trabecular bone. We show that the architecture of the femoral head trabeculae in Sciuromorpha correlates with body mass and locomotor habits. Our findings provide a new basis for experimental research focused on functional significance of bone inner microstructure.Electronic supplementary materialThe online version of this article (10.1186/s40851-018-0093-z) contains supplementary material, which is available to authorized users.

Trabecular architecture in the humeral metaphyses of non‐avian reptiles (Crocodylia, Squamata and Testudines): Lifestyle, allometry and phylogeny

“…BV/TV was also reported to be independent of body size in mammals, through various sampled bones in a wide variety of taxa (Barak, Lieberman, & Hublin, ), but also in more restricted samplings: in thoracic vertebrae of hominoids (Cotter et al, ) or in fore limb epiphyses of xenarthrans (Amson et al, ). However, other analyses have found that BV/TV had a positive allometry in the femoral epiphyses of mammals and birds (Doube et al, ), in the lumbar vertebrae of strepsirrhine primates (Fajardo et al, ), in the humeral and femoral heads of primates (Ryan & Shaw, ) and in the femoral heads of sciuromorphs (Mielke et al, ). For BV/TV, isometry or positive allometry do not seem to be associated to a particular bone (both present in vertebrae and limbs bones) or clade (both present throughout mammals), but this parameter might be correlated to other characteristics, such as locomotor postures.…”

“…Structural scaling of trabeculae: All variables were log‐transformed and allometry was investigated with linear regression of each parameter against the body size proxy, TV. In Mielke et al (), the observed scaling ( a obs ) of the regression between each trabecular parameter and VOI edge length (both log‐transformed) was compared with an expected scaling under isometry ( a iso ). As TV is a volume (unit: mm 3 ), the a iso in our analysis will be equal to the third of values from Mielke et al (), because its VOI edge length was expressed in mm.…”

“…In Mielke et al (), the observed scaling ( a obs ) of the regression between each trabecular parameter and VOI edge length (both log‐transformed) was compared with an expected scaling under isometry ( a iso ). As TV is a volume (unit: mm 3 ), the a iso in our analysis will be equal to the third of values from Mielke et al (), because its VOI edge length was expressed in mm. BV/TV and DA are dimensionless ratios for which a iso = 0 (see Table , Supporting Information, file 5).…”

“…In a study focused on the fore limb epiphyses of xenarthrans, trabeculae have shown the clearest functional signal through their anisotropy: armadillos, fully terrestrial and fossorial, have the most anisotropic trabecular architecture in xenarthrans (Amson, Arnold, van Heteren, Canoville, & Nyakatura, ). In a study focused on the sciuromorph femoral head, four trabecular parameters have shown functional signals related to the various lifestyles found in this clade (Mielke et al, ).…”

“…Thanks to the development of X‐ray computed microtomography, 3D trabecular architecture could be extensively studied in birds (e.g., Bishop et al, ; Doube, Kłosowski, Wiktorowicz‐Conroy, Hutchinson, & Shefelbine, ; Fajardo, Hernandez, & O'Connor, ; Pontzer et al, ) and mammals (e.g., many orders [Doube et al, ], bovids [Mittra, Rubin, & Qin, , Sode, Burghardt, Nissenson, & Majumdar, ], lagomorphs [Marchand, Chen, Buschmann, & Hoemann, , van der Meulen et al, ], primates [Barak, Lieberman, Raichlen, et al, , Cunningham & Black, , Kivell, Skinner, Lazenby, & Hublin, , Lazenby, Skinner, Kivell, & Hublin, , Sode et al, ], rodents [Carlson, Lublinsky, & Judex, , Lambers et al, , Sode et al, ], sciuromorphs [Mielke et al, ], suids [Ben‐Zvi, Reznikov, Shahar, & Weiner, ], and xenarthrans [Amson et al, ]). In comparison, 3D trabecular architecture of nonavian reptiles has received little attention.…”