Three‐dimensional characterization of osteocyte volumes at multiple scales, and its relationship with bone biology and genome evolution in ray‐finned fishes. (20th March 2020)

• Record Type: Journal Article
• Authors: Davesne, Donald; Schmitt, Armin D.; Fernandez, Vincent; Benson, Roger B. J.; Sanchez, Sophie
• Is Part Of: Journal of evolutionary biology. Volume 33:Number 6(2020)
• Page Start: 808
• Page End: 830
• Publication Date: 2020-03-20
• Subjects: Actinopterygii -- bone biology -- genome size -- osteocytes -- palaeogenomics -- SRµCT; Evolution (Biology) -- Periodicals; Biology -- Periodicals; 576.8
• DOI: 10.1111/jeb.13612
• Languages: English
• ISSNs: 1010-061X

Abstract

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 characterized and mostly relies on incomplete, two‐dimensional information. In this study, we characterize 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 visualization of osteocyte lacunae and direct measurement of their size (volumes). Our specimen sample is designed to characterize 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 organized 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 ninefold 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. Abstract : In this article, we images bones from 34 modern actinopterygians (ray‐finned fishes) using synchrotron micro‐CT data to image their bone cell (osteocyte) lacunae in 3D. We find that osteocytes vary in volume between areas of the same bone (e.g. between woven and lamellar bone), and between different bones of the skeleton. It it therefore necessary to compare homologous areas when comparison of osteocytle lacuna volumes has to be made. Finally, we find that, as in other vertebrates, genome size is the best explanatory variable for osteocyte volumes at the interspecific scale.This implies a great potential of these cells for actinoptergyian palaeogenomics.