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Scaling of statically derived osteocyte lacunae in extant birds: implications for palaeophysiological reconstruction.

ABSTRACT: Osteocytes are mature versions of osteoblasts, bone-forming cells that develop in two ways: via 'static' osteogenesis, differentiating and ossifying tissue in situ to form a scaffold upon which other bone can form, or 'dynamic' osteogenesis, migrating to infill or lay down bone around neurovasculature. A previous study regressed the volume of osteocyte lacunae derived from dynamic osteogenesis (DO) of a broad sample of extant bird species against body mass, the growth rate constant ( k), mass-specific metabolic rate, genome size, and erythrocyte size. There were significant relationships with body mass, growth rate, metabolic rate, and genome size, with the latter being the strongest. Using the same avian histological dataset, we measured over 3800 osteocyte lacunar axes derived from static osteogenesis (SO) in order to look for differences in the strength of form-function relationships inferred for DO-derived lacunae at the cellular and tissue levels. The relationship between osteocyte lacunar volume and body mass was stronger when measuring SO lacunae, whereas relationships between osteocyte lacunar volume versus growth rate and basal metabolic rate disappeared. The relationship between osteocyte lacuna volume and genome size remained significant and moderately strong when measuring SO lacunae, whereas osteocyte lacuna volume was still unrelated to erythrocyte size. Our results indicate that growth and metabolic rate signals are contained in avian DO but not SO osteocyte lacunae, suggesting that the former should be used in estimating these parameters in extinct animals.

SUBMITTER: Grunmeier O

PROVIDER: S-EPMC6501357 | biostudies-literature | 2019 Apr

REPOSITORIES: biostudies-literature

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Scaling of statically derived osteocyte lacunae in extant birds: implications for palaeophysiological reconstruction.

Grunmeier Orvil O D'Emic Michael D MD

Biology letters 20190401 4

Osteocytes are mature versions of osteoblasts, bone-forming cells that develop in two ways: via 'static' osteogenesis, differentiating and ossifying tissue in situ to form a scaffold upon which other bone can form, or 'dynamic' osteogenesis, migrating to infill or lay down bone around neurovasculature. A previous study regressed the volume of osteocyte lacunae derived from dynamic osteogenesis (DO) of a broad sample of extant bird species against body mass, the growth rate constant ( k), mass-sp ...[more]

PMID: 30940024

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Project description:Despite the extensive studies on biological function of osteocytes, there are limited studies that evaluated the structural role of osteocyte lacunae on local mechanical properties of the bone matrix. As a result, the goal of this study was to elucidate the independent contribution of osteocyte lacunae structure on mechanical properties and fracture behavior of the bone matrix uncoupled from its biological effects and bone tissue composition variation. This study combined cohesive finite element modeling with experimental data from a lactation rat model to evaluate the influence of osteocyte lacunar area porosity, density, size, axis ratio, and orientation on the elastic modulus, ultimate strength, and ultimate strain of the bone matrix as well as on local crack formation and propagation. It also performed a parametric study to isolate the influence of a single osteocyte lacunae structural property on the mechanical properties of the bone matrix. The experimental measurements demonstrated statistically significant differences in lacunar size between ovariectomized rats with lactation history and virgin groups (both ovariectomized and intact) and in axis ratio between rats with lactation history and virgins. There were no differences in mechanical properties between virgin and lactation groups as determined by the finite element simulations. However, there were statistically significant linear relationships between the physiological range of osteocyte lacunar area porosity, density, size, and orientation and the elastic modulus and ultimate strength of the bone matrix in virgin and lactation rats. The parametric study also revealed similar but stronger relationships between elastic modulus and ultimate strength and lacunar density, size, and orientation. The simulations also demonstrated that the osteocyte lacunae guided the crack propagation through local stress concentrations. In summary, this study enhanced the limited knowledge on the structural role of osteocyte lacunae on local mechanical properties of the bone matrix. These data are important in gaining a better understanding of the mechanical implications of the local modifications due to osteocytes in the bone matrix.

Project description:Describing and quantifying vascular canal orientation and volume of osteocyte lacunae in bone is important in studies of bone growth, mechanics, health and disease. It is also an important element in analysing fossil bone in palaeohistology, key to understanding the growth, life and death of extinct animals. Often, bone microstructure is studied using two-dimensional (2D) sections, and three-dimensional (3D) shape and orientation of structures are estimated by modelling the structures using idealised geometries based on information from their cross sections. However, these methods rely on structures meeting strict geometric assumptions. Recently, 3D methods have been proposed which could provide a more accurate and robust approach to bone histology, but these have not been tested in direct comparison with their 2D counterparts in terms of accuracy and sensitivity to deviations from model assumptions. We compared 2D and 3D methodologies for estimating key microstructural traits using a combination of experimental and idealised test data sets. We generated populations of cylinders (canals) and ellipsoids (osteocyte lacunae), varying the cross-sectional aspect ratios of cylinders and orientation of ellipsoids to test sensitivity to deviations from cylindricality and longitudinal orientation, respectively. Using published methods, based on 2D sections and 3D data sets, we estimated cylinder orientation and ellipsoid volume. We applied the same methods to six CT data sets of duck cortical bone, using the full volumes for 3D measurements and single CT slices to represent 2D sections. Using in silico test data sets that did deviate from ideal cylinders and ellipsoids resulted in inaccurate estimates of cylinder or canal orientation, and reduced accuracy in estimates of ellipsoid and lacunar volume. These results highlight the importance of using appropriate 3D imaging and quantitative methods for quantifying volume and orientation of 3D structures and offer approaches to significantly enhance our understanding of bone physiology based on accurate measures for bone microstructures.

Project description:Ancestral sequence reconstruction (ASR) is a phylogenetic method widely used to analyze the properties of ancient biomolecules and to elucidate mechanisms of molecular evolution. Despite its increasingly widespread application, the accuracy of ASR is currently unknown, as it is generally impossible to compare resurrected proteins to the true ancestors. Which evolutionary models are best for ASR? How accurate are the resulting inferences? Here we answer these questions using a cross-validation method to reconstruct each extant sequence in an alignment with ASR methodology, a method we term "extant sequence reconstruction" (ESR). We thus can evaluate the accuracy of ASR methodology by comparing ESR reconstructions to the corresponding known true sequences. We find that a common measure of the quality of a reconstructed sequence, the average probability, is indeed a good estimate of the fraction of correct amino acids when the evolutionary model is accurate or overparameterized. However, the average probability is a poor measure for comparing reconstructions from different models, because, surprisingly, a more accurate phylogenetic model often results in reconstructions with lower probability. While better (more predictive) models may produce reconstructions with lower sequence identity to the true sequences, better models nevertheless produce reconstructions that are more biophysically similar to true ancestors. In addition, we find that a large fraction of sequences sampled from the reconstruction distribution may have fewer errors than the single most probable (SMP) sequence reconstruction, despite the fact that the SMP has the lowest expected error of all possible sequences. Our results emphasize the importance of model selection for ASR and the usefulness of sampling sequence reconstructions for analyzing ancestral protein properties. ESR is a powerful method for validating the evolutionary models used for ASR and can be applied in practice to any phylogenetic analysis of real biological sequences. Most significantly, ESR uses ASR methodology to provide a general method by which the biophysical properties of resurrected proteins can be compared to the properties of the true protein.

Project description:BackgroundAmong living fliers (birds, bats, and insects), birds display relatively high aspect ratios, a dimensionless shape variable that distinguishes long and narrow vs. short and broad wings. Increasing aspect ratio results in a functional tradeoff between low induced drag (efficient cruise) and increased wing inertia (difficult takeoff). Given the wide scope of its functional effects, the pattern of aspect ratio evolution is an important factor that contributes to the substantial ecological and phylogenetic diversity of living birds. However, because the feathers that define the wingtip (and hence wingspan and aspect ratio) often do not fossilize, resolution in the pattern of avian wing shape evolution is obscured by missing information. Here I use a comparative approach to investigate the relationship between skeletal proxies of flight feather attachment and wing shape.ResultsAn accessory lobe of the internal index process of digit II-1, a bony correlate of distal primary attachment, shows weak but statistically significant relationships to aspect ratio and mass independent of other skeletal morphology. The dorsal phalangeal fossae of digit II-1, which house distal primaries VIII and IX, also show a trend of increased prominence with higher aspect ratio. Quill knobs on the ulna are examined concurrently, but do not show consistent signal with respect to wing shape.ConclusionsAlthough quill knobs are cited as skeletal correlates of flight performance in birds, their relationship to wing shape is inconsistent among extant taxa, and may reflect diverging selection pressures acting on a conserved architecture. In contrast, correlates of distal primary feather attachment on the major digit show convergent responses to increasing aspect ratio. In light of the diversity of musculoskeletal and integumentary mophology that underlies wing shape in different avian clades, it is unlikely that a single skeletal feature will show consistent predictive power across Neoaves. Confident inference of wing shape in basal ornithurine birds will require multiple lines of evidence, together with an understanding of clade-specific evolutionary trends within the crown.

Dataset Information

Scaling of statically derived osteocyte lacunae in extant birds: implications for palaeophysiological reconstruction.

Publications

Scaling of statically derived osteocyte lacunae in extant birds: implications for palaeophysiological reconstruction.

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