The phylogenetic origin and evolution of acellular bone in teleost fishes: insights into osteocyte function in bone metabolism
- Published
- Accepted
- Subject Areas
- Aquaculture, Fisheries and Fish Science, Evolutionary Studies, Paleontology, Zoology, Histology
- Keywords
- osteocyte, acellular bone, anosteocytic bone, Actinopterygii, Teleostei, Salmoniformes, Scombridae, ancestral state reconstruction, bone remodelling, endothermy
- Copyright
- © 2019 Davesne et al.
- Licence
- This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, reproduction and adaptation in any medium and for any purpose provided that it is properly attributed. For attribution, the original author(s), title, publication source (PeerJ Preprints) and either DOI or URL of the article must be cited.
- Cite this article
- 2019. The phylogenetic origin and evolution of acellular bone in teleost fishes: insights into osteocyte function in bone metabolism. PeerJ Preprints 7:e27406v2 https://doi.org/10.7287/peerj.preprints.27406v2
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.
Author Comment
This version of the manuscript has been accepted for publication in the peer-reviewed journal Biological Reviews. It includes various clarifications and corrects typos.
Supplemental Information
Table S1. Complete list of actinopterygian (ray-finned fish) taxa surveyed by our literature review, including supplementary species obtained with our SRµCT data (Table 1)
In the case of old literature, species names were often outdated. We used FishBase (Froese & Pauly, 2018) and the Catalog of Fishes (Eschmeyer, Fricke, & van der Laan, 2018) to locate the corresponding valid names.
Fig. S1. Time-calibrated multilocus tree of extant actinopterygians (ray-finned fishes), obtained from optimising bone type on the topology T1 (Near et al., 2012)
The character states are ‘cellular bone’ (in dark blue) and ‘acellular bone’ in (yellow). Character states for coded species are at the tips, and the reconstructed ancestral states at the nodes.
Fig. S2. Time-calibrated multilocus tree of extant and fossil actinopterygians (ray-finned fishes), obtained from optimising bone type on the topology T2 (Betancur-R., Ortí, & Pyron, 2015)
The character states are ‘cellular bone’ (in dark blue) and ‘acellular bone’ in (yellow). Character states for coded species are at the tips, and the reconstructed ancestral states at the nodes.
Fig. S3. Time-calibrated multilocus tree of extant actinopterygians (ray-finned fishes), obtained from optimising bone type on the topology T3 (Hughes et al., 2018)
The character states are ‘cellular bone’ (in dark blue) and ‘acellular bone’ in (yellow). Character states for coded species are at the tips, and the reconstructed ancestral states at the nodes.