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

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 propose to 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 osteocytes and direct measurement of their volumes. Our specimen sample is designed to characterise osteocyte variation at three scales: within a bone, between the bones of one individual and between taxa spanning actinopterygian phylogeny. At the intra-bone scale, we find that osteocytes vary noticeably in volume between zones of organised and woven bone (being larger in the latter), and across cyclical bone deposition. This is probably explained by differences in bone deposition rate, with larger osteocytes contained in bone that deposits faster. Osteocyte volumes vary from one bone to another, for unclear reasons. Finally, we find that genome size is the best explanatory variable of osteocyte volume at the inter-specific scale: actinopterygian taxa with larger genomes (polyploid taxa in particular) have larger osteocytes. Our findings corroborate previous two-dimensional observations in tetrapods, and open new perspectives for actinopterygian bone evolution, physiology and palaeogenomics.

The relationship between genome size and metabolic rate in extant vertebrates

“…Furthermore, Maciak et al [43] cite previous studies that failed to find differences in SMR in di-and triploids of other teleost hybrids. An unpublished study on actinopterygians also suggest that genome size and ploidy level are individually correlated with bone osteocyte lacunae volume, tested separately for data measured from dentaries and ribs [44]. These results suggest that genome size influences various biological attributes in actinopterygians but not necessarily metabolic rate.…”