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Data for: Three-dimensional characterization of osteocyte volumes at multiple scales, and its relationship with bone biology and genome evolution in ray-finned fishes

Citation

Davesne, Donald et al. (2021), Data for: Three-dimensional characterization of osteocyte volumes at multiple scales, and its relationship with bone biology and genome evolution in ray-finned fishes, Dryad, Dataset, https://doi.org/10.5061/dryad.xksn02vc2

Abstract

Osteocytes, cells embedded within the bone mineral matrix, inform on key aspects of vertebrate biology. In particular, a relationship between volumes of the osteocytes and bone growth and/or genome size has been proposed for several tetrapod lineages. However, the variation in osteocyte volume across different scales is poorly characterised, and mostly relies on incomplete, two-dimensional information. In this study, we characterise the variation of osteocyte volumes in ray-finned fishes (Actinopterygii), a clade including more than half of modern vertebrate species in which osteocyte biology is poorly known. We use X-ray synchrotron micro-computed tomography (SRµCT) to achieve a three-dimensional visualisation of osteocyte lacunae and direct measurement of their size (volumes). Our specimen sample is designed to characterise variation in osteocyte lacuna morphology at three scales: within a bone, among the bones of one individual and among species. At the intra-bone scale, we find that osteocyte lacunae vary noticeably in size between zones of organised and woven bone (being up to six times larger in woven bone), and across cyclical bone deposition. This is probably explained by differences in bone deposition rate, with larger osteocyte lacunae contained in bone that deposits faster. Osteocyte lacuna volumes vary 3.5-fold among the bones of an individual, and this cannot readily be explained by variation in bone growth rate or other currently observable factors. Finally, we find that genome size provides the best explanation of variation in osteocyte lacuna volume among species: actinopterygian taxa with larger genomes (polyploid taxa in particular) have larger osteocyte lacunae (with a nine-fold variation in median osteocyte volume being measured). Our findings corroborate previous two-dimensional studies in tetrapods that also observed similar patterns of intra-individual variation and found a correlation with genome size. This opens new perspectives for further studies on bone evolution, physiology and palaeogenomics in actinopterygians, and vertebrates as a whole.

Methods

These data sheets (in the .csv format) are generated from the software VGStudioMax. They stem from the segmenting of tomograms (digital 'slices') obtained with PPC-SRµCT (synchrotron microtomography) of modern ray-finned fish bones. The osteocyte lacunae (bone cell spaces) were segmented out of the bone mineral matrix, and analysed with the 'Porosity/Inclusion' module to automatically obtain a set of measurements. These include (but are not limited to): osteocyte lacuna volumes (µm³), position in the x, y and z axis and range of tomogram gray values.

Each data sheet corresponds to one set of segmented objects (osteocytes lacunae and a few, mostly smaller, unidentified objects) from each PPC-SRµCT tomogram (list of specimens and scans in the accompanying article), with two segmenting thresholds ('min' and 'max') for each tomogram.

The name of each file corresponds to the following convention:  'Genus name' _ 'Species name' _ 'Specimen number'_ 'Bone' _ 'Location in bone (when appropriate)' _ 'Segmenting threshold'

Funding

Leverhulme Trust, Award: RPG-2016-168