The phylogenetic origin and evolution of acellular bone in teleost fishes: insights into osteocyte function in bone metabolism

Abstract

Vertebrate bone is composed of three main cell types, the most prominent of which are the osteocytes. These cells are thought to play a fundamental role in bone physiology, however they are entirely absent in most extant species of teleosts, a group that comprises the vast majority of bony ‘fishes’, and approximately half of vertebrates. Understanding how this acellular (anosteocytic) bone appeared and was maintained in such an important vertebrate group has important implications for our understanding of the function and evolution of osteocytes. Nevertheless, although it is clear that cellular bone is ancestral for teleosts, it has not been clear in which specific subgroup the osteocytes were lost. This review aims at clarifying the phylogenetic distribution of cellular and acellular bone in teleosts, to identify its precise origin, reversals to cellularity, and their implications. We surveyed the bone type for more than 600 ray-finned fish species, fossil and extant and optimised the results on recent large-scale molecular phylogenetic trees, estimating ancestral states. We find that acellular bone is a probable synapomorphy of Euteleostei, a group uniting approximately two-thirds of teleost species. We also confirm homoplasy in these traits: acellular bone occurs in some non-euteleosts (though rarely), and cellular bone was reacquired several times independently within euteleosts, in salmons and relatives, tunas and the opah. The occurrence of peculiar ecological (e.g., anadromous migration) and physiological (e.g., red-muscle endothermy) strategies in these lineages might explain the reacquisition of osteocytes. Our review supports that the main contribution of osteocytes in teleost bone is to mineral homeostasis (via osteocytic osteolysis) and not to strain detection or bone remodelling, helping to clarify their role in bone physiology.

Short-term effects of estradiol and bisphenol A on gene expression associated with early head mineralization in the seabass Dicentrarchus labrax

“…The European seabass Dicentrarchus labrax is a non-model species of high commercial interest for fisheries and aquaculture where skeletal malformations are a major issue. Although osteoblasts never turn into osteocytes in this species (Kranenbarg et al, 2005;Davesne et al, 2018), mononuclear osteoclasts are still present (Boglione et al, 2013) and the head skeleton development involves cartilage growth and ossification (Darias et al, 2010). In this study, we investigated whether waterborne exposure to (xeno)estrogens impacts early head mineralization in Dicentrarchus labrax.…”

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“…Heat production by red muscles involved in swimming (rather than modified ocular 835 muscles) and redistribution in a large proportion of the body (rather than in the brain 836 region only) is the key distinction between red-muscle and cranial endothermy. Given 837 that both acanthomorph lineages that developed red-muscle endothermy are also the 838 only ones that reacquired osteocytes, a correlation between these characters is likely 839 (Davesne et al, 2018). As for salmoniforms, we can hypothesise that the correlation 840 stems from an intense muscular activity associated with sustained swimming.…”

“…(3) Finally, the reacquisition of 780 osteocytes does not seem to be linked with structural homeostasis: bone in tunas, opah 781 and billfishes appears to have active, intense and sustained resorption and remodelling 782 activities (Fig. 5B, D, E) Conversely, a correlation between cellular bone and endothermy in acanthomorphs 788 appears to be more substantiated (Meunier, 1987;Ricqlès et al, 1991;Meunier & 789 Huysseune, 1992; Davesne et al, 2018). Our new SRµCT data confirm that cellular 790 bone co-occurs with a modification in the distribution and position of the lateral aerobic 791 red muscles (Fig.…”