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Abstract Linking morphology and function is critical to understanding the evolution of organismal shape. Performance landscapes, or performance surfaces, associate empirical functional performance data with a morphospace to assess how shape variation relates to functional variation. Performance surfaces for multiple functions also can be combined to understand the functional trade‐offs that affect the morphology of a particular structure across species. However, morphological performance surfaces usually require empirical determination of performance for a number of theoretical shapes that are evenly distributed throughout the morphospace. This process is time‐consuming, and is problematic for structures that are difficult to precisely manipulate.We sought to (a) understand the degree and pattern of sampling required to produce a reliable and nuanced performance surface and (b) investigate the possibility of building a surface using only naturally occurring morphologies. To do this, we subsampled a pre‐existing set of turtle shell performance surfaces in four different ways: first, uniform subsampling of theoretical morphologies across the surface; second, random subsampling of theoretical morphologies across the surface; third, a combination uniform/random subsampling method called close‐pairs sampling and fourth, subsampling only points on the surface known to correspond to a naturally occurring turtle shell morphology. Each subset was interpolated with ordinary Kriging to produce a new performance surface for comparison to the original.We found that using a fraction of the theoretical morphologies examined in the original study (half as many or fewer) was sufficient to produce a performance surface bearing close resemblance to the original (Pearson correlation ≥0.90); close‐pairs sampling dramatically increased the power of small sample sizes. We also discovered that only sampling points on the surface corresponding to naturally occurring morphologies produced an accurate surface, but results were better when individual specimens, rather than species averages, were used.Our findings demonstrate the viability of using performance surfaces to understand the evolution of complex morphologies for which theoretical shape modelling is difficult or computationally burdensome. Both lower levels of carefully configured sampling throughout the theoretical morphospace, and development of performance surfaces using only data from naturally occurring morphologies, are acceptable alternatives to the dense theoretical shape sampling employed in previous studies. ​ 

Captive specimens in museum collections facilitate study of rare taxa, but the lifestyles, diets, and lifespans of captive animals differ from their wild counterparts. Trabecular bone architecture adapts to in vivo forces, and may reflect interspecific variation in ecology and behavior as well as intraspecific variation between captive and wild specimens. We compared trunk vertebrae bone microstructure in captive and wild xenarthran mammals to test the effects of ecology and captivity. We collected μCT scans of the last six presacral vertebrae in 13 fossorial, terrestrial, and suspensorial xenarthran species (body mass: 120 g to 35 kg). For each vertebra, we measured centrum length; bone volume fraction (BV.TV); trabecular number and mean thickness (Tb.Th); global compactness (GC); cross-sectional area; mean intercept length; star length distribution; and connectivity and connectivity density. Wild specimens have more robust trabeculae, but this varies with species, ecology, and pathology. Wild specimens of fossorial taxa (Dasypus) have more robust trabeculae than captives, but there is no clear difference in bone microstructure between wild and captive specimens of suspensorial taxa (Bradypus, Choloepus), suggesting that locomotor ecology influences the degree to which captivity affects bone microstructure. Captive Tamandua and Myrmecophaga have higher BV.TV, Tb.Th, and GC than their wild counterparts due to captivity-caused bone pathologies. Our results add to the understanding of variation in mammalian bone microstructure, suggest caution when including captive specimens in bone microstructure research, and indicate the need to better replicate the habitats, diets, and behavior of animals in captivity. 

Captive specimens in natural history collections allow researchers to inspect the morphologies of rare taxa, but the lifestyles,diets, and lifespans of captive animals differ from those of their wild counterparts. To quantify these differences, we compared bone microstructure of trunk vertebrae in captive and wild xenarthran mammals (sloths, armadillos, anteaters). Because trabecular bone architecture (TBA) adapts to in vivo forces, bone microstructure reflects ecology and behavior, but this means that it may differ between captive and wild specimens of the same species. We collected μCT scans of the last six presacral vertebrae in 13 species of fossorial, terrestrial, and suspensorial xenarthrans ranging in body mass from 120g (Chlamyphorus) to 35kg (Myrmecophaga). For each vertebra, we measured bone volume fraction (BVF); trabecular number, mean thickness (TbTh), and orientation; global compactness; and cross sectional area. Wild specimens generally have more robust trabeculae, but this differs based on species, vertebral position, ecology, and pathology. The wild specimens of fossorial taxa (Dasypus) have more robust trabeculae than their captive counterparts, but there is no clear difference in TBA of wild and captive specimens in suspensorial and terrestrial taxa (Bradypus, Choloepus, Cyclopes). These data suggest that locomotor ecology affects the level to which captivity affects bone microstructure. The captive specimens of both Tamandua and Myrmecophaga have higher BVF and TbTh than their wild counterparts, indicating more brittle trabeculae due to bone pathologies caused by captivity. Our results add to the overall understanding of variation in mammalian bone microstructure and suggest caution when including captive specimens in research on TBA. 

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. 

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. 

Captive (zoo) specimens in natural history collections allow researchers to inspect the morphologies of rare or CITES-listed taxa, but the lifestyles, diets, and lifespans of captive animals differ from those of their wild counterparts. To quantify these differences, we compared trabecular bone architecture (TBA) of dorsal vertebrae in captive and wild specimens of xenarthran mammals (anteaters, armadillos, and sloths). Because TBA develops following in-vivo bone force regimes, it reflects ecology and behavior, but this also means that it may differ between captive and wild specimens of the same species. We collected μCT scans of the last six presacral vertebrae in 15 species of fossorial, terrestrial, and suspensorial xenarthrans ranging in body mass from 120g (Chlamyphorus) to 35kg (Myrmecophaga). For each vertebra, we measured bone volume fraction (BVF), trabecular number (TbN), mean trabecular thickness (TbTh), degree of anisotropy, and trabecular orientation. We found that wild specimens generally have a greater BVF, TbN, and TbTh than captive specimens, but that these metrics differ by species, vertebral position, ecology, and pathology. Wild specimens of Dasypus have greater BVF, TbN, and TbTh than captive specimens in the three most posterior lumbar vertebrae, but have much closer metrics in the anterior three vertebrae. In Choloepus, BVF, TbN, and TbTn are greater in wild specimens in the anterior vertebrae and more similar in the posterior vertebrae. Arthritis in captive Tamandua increased BVF and TbTh, whereas wild specimens had greater TbN. Our results add to overall understanding of variation in mammalian vertebral trabecular bone, and suggest caution when including captive specimens in research on the relationship between TBA and ecology. 

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.