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: osteoblasts, osteoclasts and osteocytes, the latter being by far the most numerous. Osteocytes are thought to play a fundamental role in bone physiology and homeostasis, 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 to clarify 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 fossil and extant ray-finned fish species 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 (although rarely), and cellular bone was reacquired several times independently within euteleosts, in salmons and relatives, tunas and the opah (Lampris sp.). 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.

Bony lesions in early tetrapods and the evolution of mineralized tissue repair

“…A recent evolutionary analysis suggested that aspidin was the ancestral bone type, with cellular bone evolving from it at least two times in vertebrate evolution (Keating et al 2018). Cellular bone first evolved in osteostracans, and its presence in placoderms, acanthodians, and osteichthyans suggests that cellular bone is a synapomorphy of gnathostomes and osteostracans (Brazeau and Friedman 2014;Davesne et al 2019). Because a healing mechanism is found in both aspidin and cellular bone, and cellular bone evolved from aspidin, it is most parsimonious that the healing mechanism evolved in early vertebrate bone (regardless of its cellularity).…”

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

“…The clade Euteleostei includes approximately two‐thirds of teleost diversity (Nelson, Grande, & Wilson, 2016), yet is only represented by salmoniforms in our sample. This is because most euteleosts show ‘acellular’ (or anosteocytic) bone that is entirely devoid of osteocytes (Davesne, Meunier, Friedman, Benson, & Otero, 2018; Davesne et al, 2019; Kölliker, 1859; Meunier, 1989; Moss, 1961; Parenti, 1986; Shahar & Dean, 2013). Salmoniforms are one of the few exceptions, and may have re‐acquired osteocytes secondarily during their early evolution (Davesne et al, 2019).…”

“…Characterizing the variation in osteocyte morphology is fundamental to constraining hypotheses about its biological causes, and can therefore provide insights into the multiple functions of osteocytes in living bone, which are currently not entirely understood in ray‐finned fishes (Currey, Dean, & Shahar, 2017; Davesne et al, 2019; Doherty, Ghalambor, & Donahue, 2015; Shahar & Dean, 2013). There are many accounts of variation in osteocyte morphology at different scales, mostly within various vertebrate lineages other than actinopterygians: (a) within a single bone (e.g.…”

“…Finally, with a few exceptions (e.g. Amprino & Godina, 1956; Davesne et al, 2019; Kölliker, 1859; Meunier, 1989; Meunier & Huysseune, 1992; Stéphan, 1900), interspecific comparisons of osteocyte morphology have been made only on tetrapods (four‐limbed terrestrial vertebrates), representing only a subset of vertebrate diversity.…”

Toward an “Ancient” Virtual World: Improvement Methods on X-ray CT Data Processing and Virtual Reconstruction of Fossil Skulls

“…All these virtual techniques are based on the 3D characterization of the object (e.g., skull, mandibles, or any other skeletal part preserved as a fossil or footprints and burrow casts) subject to analysis (Knaust, 2012;Kouraiss et al, 2019). This could be also done to digitize solely the external surface of the object (e.g., using laser scanning, modulated-light, structurelight surface scanning or photogrammetry) or to digitize both the external surface as well as the internal structures with XCT (Kouraiss et al, 2019) or synchrotron microtomography (SRµCT) (Sanchez et al, 2012;Davesne et al, 2019;Honkanen et al, 2020). Depending on the type of the object and the aim of the study, the resolution required will be different, and therefore, one type of tomography will be used.…”