The regionalization of the mammalian spinal column is an important evolutionary, developmental, and functional hallmark of the clade. Vertebral column regions are usually defined using transitions in external bone morphology, such as the presence of transverse foraminae or rib facets, or measurements of vertebral shape. Yet the internal structure of vertebrae, specifically the trabecular (spongy) bone, plays an important role in vertebral function, and is subject to the same variety of selective, functional, and developmental influences as external bone morphology. Here, we investigated regionalization of external and trabecular bone morphology in the vertebral column of a group of shrews (family Soricidae). The primary goals of this study were to: (1) determine if vertebral trabecular bone morphology is regionalized in large shrews, and if so, in what configuration relative to external morphology; (2) assess correlations between trabecular bone regionalization and functional or developmental influences; and (3) determine if external and trabecular bone regionalization patterns provide clues about the function of the highly modified spinal column of the hero shrew Scutisorex. Trabecular bone is regionalized along the soricid vertebral column, but the configuration of trabecular bone regions does not match that of the external vertebral morphology, and is less consistent across individuals and species. The cervical region has the most distinct and consistent trabecular bone morphology, with dense trabeculae indicative of the ability to withstand forces in a variety of directions. Scutisorex exhibits an additional external morphology region compared to unmodified shrews, but this region does not correspond to a change in trabecular architecture. Although trabecular bone architecture is regionalized along the soricid vertebral column, and this regionalization is potentially related to bone functional adaptation, there are likely aspects of vertebral functional regionalization that are not detectable using trabecular bone morphology. For example, the external morphology of the Scutisorex lumbar spine shows signs of an extra functional region that is not apparent in trabecular bone analyses. It is possible that body size and locomotor mode affect the degree to which function is manifest in trabecular bone, and broader study across mammalian size and ecology is warranted to understand the relationship between trabecular bone morphology and other measures of vertebral function such as intervertebral range of motion.
The sacrum occupies a functionally important anatomical position as part of the pelvic girdle and vertebral column. Sacral orientation and external morphology in modern humans are distinct from those in other primates and compatible with the demands of habitual bipedal locomotion. Among nonhuman primates, however, how sacral anatomy relates to positional behaviors is less clear. As an alternative to evaluation of the sacrum's external morphology, this study assesses if the sacrum's internal morphology (i.e., trabecular bone) differs among extant primates. The primary hypothesis tested is that trabecular bone parameters with established functional relevance will differ in the first sacral vertebra (S1) among extant primates that vary in positional behaviors. Results for analyses of individual variables demonstrate that bone volume fraction, degree of anisotropy, trabecular number, and size‐corrected trabecular thickness differ among primates grouped by positional behaviors to some extent, but not always in ways consistent with functional expectations. When examined as a suite, these trabecular parameters distinguish obligate bipeds from other positional behavior groups; and, the latter three trabecular bone variables further distinguish knuckle‐walking terrestrial quadrupeds from manual suspensor‐brachiators, vertical clingers and leapers, and arboreal quadrupeds, as well as between arboreal and terrestrial quadrupeds. As in other regions of the skeleton in modern humans, trabecular bone in S1 exhibits distinctively low bone volume fraction. Results from this study of extant primate S1 trabecular bone structural variation provide a functional context for interpretations concerning the positional behaviors of extinct primates based on internal sacral morphology. Anat Rec, 302:1354–1371, 2019. © 2018 Wiley Periodicals, Inc.
more » « less- NSF-PAR ID:
- 10456574
- Publisher / Repository:
- Wiley Blackwell (John Wiley & Sons)
- Date Published:
- Journal Name:
- The Anatomical Record
- Volume:
- 302
- Issue:
- 8
- ISSN:
- 1932-8486
- Page Range / eLocation ID:
- p. 1354-1371
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
more » « less
Synopsis -
The regionalized vertebral column is a hallmark of mammalian morphology and reflects functional differentiation of the vertebral regions. Mammalian vertebrae are serially homologous and morphologically patterened by Hox expression, but also vary in number and gross morphology across species. The trabecular bone inside vertebral centra is more plastic than gross vertebral bone, and structurally adapts to better withstand forces it experiences during life. However, the functional regionalization of vertebral trabecular bone is poorly examined. Are there trabecular "regions” reflecting the differing functions and in-vivo stress patterns of gross morphological vertebral regions? Or is trabecular morphology homogeneous throughout the spine, suggesting that differences in functional demands are borne exclusively by external characteristics? To address these questions, we collected μCT scans and linear measurements of cervical, thoracic, and lumbar vertebrae in four species of large shrews, including two species of the hero shrew Scutisorex, which has a highly modified vertebral column. We compared linear measurements and trabecular bone characteristics of the cranial and caudal ends of each centrum across species. To detect unique vertebral regions, we executed principal coordinates analysis and segmented regression on three versions of our data set: trabecular bone data only, external measurements only, and the two combined. We found that some regionalization is recovered using only trabecular bone data, but trabecular bone regions do not correspond exactly to gross vertebral regions. This reflects divergence between the functional signals of internal and external vertebral bone morphology, which should be further examined in a kinematic context.more » « less
-
more » « less
ABSTRACT The third metacarpal has been a focus of study when examining questions surrounding early hominin locomotion since this bone is adapted to the diverse range of positional behaviors performed by extant hominoids. The shape of this bone is potentially under strong selective pressure related to the biomechanical demands of terrestrial knuckle‐walking, arboreal clambering, and brachiation performed by extant hominoids since the hand directly interacts with the substrate during the performance of these movements. The objective of the present study was to explore shape variation of the third metacarpal and examine how different parts of the bone discriminated between hominoid genera that perform these different locomotor behaviors. In addition to examining general interspecies variation, shape analysis was applied to testing the knuckle‐walking hypothesis for human evolution. Fourteen 3D landmark coordinates were collected on hominoid third metacarpals, and principal component analysis and Procrustes distances were used to examine metacarpal shape. Comparable measurements were collected on fossilized third metacarpals of
Australopithecus afarensis as an early hominin test case for examining the knuckle‐walking hypothesis. Analyses that included landmarks collected on both ends of the bone distinguished humans from great apes and presented a strong functional signal related to suspensory locomotion among nonhuman hominoids, whereas the distal articular surface provided the strongest knuckle‐walking signal. The shapes ofAustralopithecus afarensis metacarpals examined in the current study did not provide evidence for a trajectory of shape change in early hominin evolution that started from a metacarpal adapted for terrestrial knuckle‐walking. Anat Rec, 302:983–998, 2019. © 2018 Wiley Periodicals, Inc. -
more » « less
Abstract Among human and nonhuman apes, calcaneal morphology exhibits significant variation that has been related to locomotor behavior. Due to its role in weight‐bearing, however, both body size and locomotion may impact calcaneal morphology. Determining how calcaneal morphologies vary as a function of body size is thus vital to understanding calcaneal functional adaptation. Here, we study calcaneus allometry and relative size in humans (
n = 120) and nonhuman primates (n = 278), analyzing these relationships in light of known locomotor behaviors. Twelve linear measures and three articular facet surface areas were collected on calcaneus surface models. Body mass was estimated using femoral head superoinferior breadth. Relationships between calcaneal dimensions and estimated body mass were analyzed across the sample using phylogenetic least squares regression analyses (PGLS). Differences between humans and pooled nonhuman primates were tested using RMA ANCOVAs. Among (and within) genera residual differences from both PGLS regressions and isometry were analyzed using ANOVAs with post hoc multiple comparison tests. The relationships between all but two calcaneus dimensions and estimated body mass exhibit phylogenetic signal at the smallest taxonomic scale. This signal disappears when reanalyzed at the genus level. Calcaneal morphology varies relative to both body size and locomotor behavior. Humans have larger calcanei for estimated body mass relative to nonhuman primates as a potential adaptation for bipedalism. More terrestrial taxa exhibit longer calcaneal tubers for body mass, increasing the triceps surae lever arm. Among nonhuman great apes, more arboreal taxa have larger cuboid facet surface areas for body mass, increasing calcaneocuboid mobility. -
more » « less
Synopsis Since their appearance in the fossil record 34 million years ago, modern cetaceans (dolphins, whales, and porpoises) have radiated into diverse habitats circumglobally, developing vast phenotypic variations among species. Traits such as skeletal morphology and ecologically linked behaviors denote swimming activity; trade-offs in flexibility and rigidity along the vertebral column determine patterns of caudal oscillation. Here, we categorized 10 species of cetaceans (families Delphinidae and Kogiidae; N = 21 animals) into functional groups based on vertebral centra morphology, swimming speeds, diving behavior, and inferred swimming patterns. We quantified trabecular bone mechanical properties (yield strength, apparent stiffness, and resilience) among functional groups and regions of the vertebral column (thoracic, lumbar, and caudal). We extracted 6 mm3 samples from vertebral bodies and tested them in compression in 3 orientations (rostrocaudal, dorsoventral, and mediolateral) at 2 mm min−1. Overall, bone from the pre-fluke/fluke boundary had the greatest yield strength and resilience, indicating that the greatest forces are translated to the tail during caudal oscillatory swimming. Group 1, composed of 5 shallow-diving delphinid species, had the greatest vertebral trabecular bone yield strength, apparent stiffness, and resilience of all functional groups. Conversely, Group 3, composed of 2 deep-diving kogiid species, had the least strong, stiff, and resilient bone, while Group 2 (3 deep-diving delphinid species) exhibited intermediate values. These data suggest that species that incorporate prolonged glides during deep descents in the water column actively swim less, and place relatively smaller loads on their vertebral columns, compared with species that execute shallower dives. We found that cetacean vertebral trabecular bone properties differed from the properties of terrestrial mammals; for every given bone strength, cetacean bone was less stiff by comparison. This relative lack of material rigidity within vertebral bone may be attributed to the non-weight-bearing locomotor modes of fully aquatic mammals.
