Three-dimensional characterization of osteocyte volumes at multiple scales, and its relationship with bone biology and genome evolution in ray-finned fishes
- 1 June 2020
- journal article
- research article
- Published by Oxford University Press (OUP) in Journal of Evolutionary Biology
- Vol. 33 (6), 808-830
- https://doi.org/10.1111/jeb.13612
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 (SR mu CT) 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.Keywords
Funding Information
- Leverhulme Trust (RPG‐2016‐168)
This publication has 119 references indexed in Scilit:
- Variation of osteocyte lacunae size within the tetrapod skeleton: implications for palaeogenomicsBiology Letters, 2011
- The amazing osteocyteJournal of Bone and Mineral Research, 2010
- Sauropod dinosaurs evolved moderately sized genomes unrelated to body sizeProceedings Of The Royal Society B-Biological Sciences, 2009
- Did genome duplication drive the origin of teleosts? A comparative study of diversification in ray-finned fishesBMC Evolutionary Biology, 2009
- Palaeogenomics of pterosaurs and the evolution of small genome size in flying vertebratesBiology Letters, 2008
- Tomographic techniques for the study of exceptionally preserved fossilsProceedings Of The Royal Society B-Biological Sciences, 2008
- Eukaryotic genome size databasesNucleic Acids Research, 2006
- Phylogenetic Timing of the Fish-Specific Genome Duplication Correlates with the Diversification of Teleost FishJournal of Molecular Evolution, 2004
- Phylogenies and the Comparative Method: A General Approach to Incorporating Phylogenetic Information into the Analysis of Interspecific DataThe American Naturalist, 1997
- Phylogenies and the Comparative MethodThe American Naturalist, 1985