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

dc.contributor.authorDavesne, Donald
dc.contributor.authorMeunier, François J.
dc.contributor.authorSchmitt, Armin D.
dc.contributor.authorFriedman, Matt
dc.contributor.authorOtero, Olga
dc.contributor.authorBenson, Roger B. J.
dc.date.accessioned2019-08-09T17:14:26Z
dc.date.availableWITHHELD_13_MONTHS
dc.date.available2019-08-09T17:14:26Z
dc.date.issued2019-08
dc.identifier.citationDavesne, Donald; Meunier, François J. ; Schmitt, Armin D.; Friedman, Matt; Otero, Olga; Benson, Roger B. J. (2019). "The phylogenetic origin and evolution of acellular bone in teleost fishes: insights into osteocyte function in bone metabolism." Biological Reviews 94(4): 1338-1363.
dc.identifier.issn1464-7931
dc.identifier.issn1469-185X
dc.identifier.urihttps://hdl.handle.net/2027.42/150563
dc.description.abstractVertebrate 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.
dc.publisherBlackwell Publishing Ltd
dc.publisherWiley Periodicals, Inc.
dc.subject.otherSalmoniformes
dc.subject.otherScombridae
dc.subject.otherancestral state reconstruction
dc.subject.otheracellular bone
dc.subject.otherendothermy
dc.subject.otherosteocyte
dc.subject.otherbone remodelling
dc.subject.otheranosteocytic bone
dc.subject.otherActinopterygii
dc.subject.otherTeleostei
dc.titleThe phylogenetic origin and evolution of acellular bone in teleost fishes: insights into osteocyte function in bone metabolism
dc.typeArticle
dc.rights.robotsIndexNoFollow
dc.subject.hlbsecondlevelEcology and Evolutionary Biology
dc.subject.hlbtoplevelScience
dc.description.peerreviewedPeer Reviewed
dc.description.bitstreamurlhttps://deepblue.lib.umich.edu/bitstream/2027.42/150563/1/brv12505-sup-0001-FigureS1.pdf
dc.description.bitstreamurlhttps://deepblue.lib.umich.edu/bitstream/2027.42/150563/2/brv12505-sup-0003-FigureS3.pdf
dc.description.bitstreamurlhttps://deepblue.lib.umich.edu/bitstream/2027.42/150563/3/brv12505-sup-0002-FigureS2.pdf
dc.description.bitstreamurlhttps://deepblue.lib.umich.edu/bitstream/2027.42/150563/4/brv12505.pdf
dc.description.bitstreamurlhttps://deepblue.lib.umich.edu/bitstream/2027.42/150563/5/brv12505_am.pdf
dc.identifier.doi10.1111/brv.12505
dc.identifier.sourceBiological Reviews
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