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 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 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 characterisation 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 et al, 2016), yet is only represented by salmoniforms in the sample. This is because euteleosts evolved 'acellular' (or anosteocytic) bone that is entirely devoid of osteocytes (Kölliker, 1859;Moss, 1961;Parenti, 1986;Meunier, 1989;Shahar & Dean, 2013;Davesne et al, 2018Davesne et al, , 2019. Salmoniforms are one of the few exceptions, and may have re-acquired osteocytes secondarily during their early evolution (Davesne et al, 2019).…”

“…Characterising 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, currently not entirely understood in ray-finned fishes (Shahar & Dean, 2013;Doherty et al, 2015;Currey et al, 2017;Davesne et al, 2019). There are many accounts of variation in osteocyte morphology at different scales within various vertebrate lineages: (1) within a single bone (e.g.…”

“…Finally, with a few exceptions (e.g. Kölliker, 1859;Stéphan, 1900;Amprino & Godina, 1956;Meunier, 1989;Meunier & Huysseune, 1992;Sanchez et al, 2014;Kamska et al, 2018;Davesne et al, 2019;Ofer et al, 2019), inter-specific comparisons of osteocyte morphology have been made only on tetrapods (four-limbed terrestrial vertebrates), representing only a subset of vertebrate diversity.…”

Exercise‐induced lordosis in zebrafish Danio rerio (Hamilton, 1822)

“…Similarly, all advanced teleosts lack osteocytes even as adults. Thus, it has been suggested that alternative, osteocyte‐independent, mechanisms of bone regulation exist (Davesne et al ., 2019; Ofer et al ., 2019; Witten & Hall, 2015; Witten & Huysseune, 2009).…”