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.
Adventures inside shrew vertebrae: trabecular bone morphology and regionalization in Soricidae
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.
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- Award ID(s):
- 1811627
- NSF-PAR ID:
- 10309650
- Date Published:
- Journal Name:
- Integrative and comparative biology
- Volume:
- 61
- Issue:
- Supplement_1
- ISSN:
- 1557-7023
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Synopsis -
In addition to having unique extra articulations on its vertebrae, the hero shrew (Scutisorex) is unusual in having almost twice as many lumbar vertebrae as other shrews of its size. Other than being noted in descriptive literature, this increase in vertebral number has received little attention; there has been no investigation of how it might reflect the elusive function of the highly modified Scutisorex spine. Comparisons of individual vertebrae and whole-column characteristics between Scutisorex and other large shrews are also lacking, despite the fact that such studies could give insight into i) function of particular vertebral regions in shrews with and without external vertebral modifications, and ii) developmental patterns driving regional proportions. We collected μCT scans and linear measurements of cervical, thoracic, and lumbar vertebrae in two species of Scutisorex and three other species of large shrews. We compared a variety of linear vertebra measurements, and trabecular bone characteristics of each centrum, across species. Further, using this combined suite of measurements, we executed principal coordinates analysis and segmented regression to detect unique vertebral regions in each taxon. Our results show that relative to other large shrews, Scutisorex has a shorter thoracic region and longer lumbar region, and, despite having more dorsal vertebrae than other species, does not have a proportionally longer body length. Regionalization signals vary within and across the five species, but generally suggest that functional regions may not correspond exactly with traditionally recognized anatomical regions of the column, and that the extended lumbar region in Scutisorex may afford it an additional functional region.more » « less
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Synopsis Trabecular bone is a spongy bone tissue that serves as a scaffolding-like support inside many skeletal elements. Previous research found allometric variation in some aspects of trabecular bone architecture (TBA) and bone microstructure, whereas others scale isometrically. However, most of these studies examined very wide size and phylogenetic ranges or focused exclusively on primates or lab mice. We examined the impact of body size on TBA across a smaller size range in the mammalian clade Xenarthra (sloths, armadillos, and anteaters). We µCT-scanned the last six presacral vertebrae of 23 xenarthran specimens (body mass 120 g–35 kg). We collected ten gross-morphology measurements and seven TBA metrics and analyzed them using phylogenetic and nonphylogenetic methods. Most metrics had similar allometries to previous work. However, because ecology and phylogeny align closely in Xenarthra, the phylogenetic methods likely removed some covariance due to ecology; clarifying the impact of ecology on TBA in xenarthrans requires further work. Regressions for Folivora had high P-values and low R-squared values, indicating that the extant sloth sample either is too limited to determine patterns or that the unique way sloths load their vertebral columns causes unusually high TBA variation. The southern three-banded armadillo sits far below the regression lines, which may be related to its ability to roll into a ball. Body size, phylogeny, and ecology impact xenarthran TBA, but parsing these effects is highly complex.
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Biological structures with extreme morphologies are puzzling because they often lack obvious functions and stymie comparisons to homologous or analogous features with more typical shapes. An example of such an extreme morphotype is the uniquely modified vertebral column of the hero shrew Scutisorex , which features numerous accessory intervertebral articulations and massively expanded transverse processes. The function of these vertebral structures is unknown, and it is difficult to meaningfully compare them to vertebrae from animals with known behavioural patterns and spinal adaptations. Here, we use trabecular bone architecture of vertebral centra and quantitative external vertebral morphology to elucidate the forces that may act on the spine of Scutisorex and that of another large shrew with unmodified vertebrae ( Crocidura goliath ). X-ray micro-computed tomography (µCT) scans of thoracolumbar columns show that Scutisorex thori is structurally intermediate between C. goliath and S. somereni internally and externally, and both Scutisorex species exhibit trabecular bone characteristics indicative of higher in vivo axial compressive loads than C. goliath. Under compressive load, Scutisorex vertebral morphology is adapted to largely restrict bending to the sagittal plane (flexion). Although these findings do not solve the mystery of how Scutisorex uses its byzantine spine in vivo , our work suggests potentially fruitful new avenues of investigation for learning more about the function of this perplexing structure.more » « less
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