doi: 10.1098/rsbl.2018.0270.
Histology of the endothermic opah (Lampris sp.) suggests a new structure-function relationship in teleost fish bone
Affiliations
- PMID:29950318
- PMCID: PMC6030602
- DOI: 10.1098/rsbl.2018.0270
Item in Clipboard
Histology of the endothermic opah (Lampris sp.) suggests a new structure-function relationship in teleost fish bone
Donald Davesne et al. Biol Lett.2018 Jun.
Display options
Format
Display options
Format
Abstract
Endothermy, production and retention of heat by the body, appeared convergently in mammals, birds and four spiny-rayed teleost fish lineages. Of these, red-muscle endothermy over most or all of the body has only appeared in two groups: tunas and the opah (Lampris). Hitherto, tunas have been the only spiny-rayed fishes known to have bones containing embedded osteocyte cells; others have acellular bone. We examined bone histology inLampris for the first time, demonstrating the presence of cellular bone very similar to that of tunas. This contrasts with the acellular condition of its ectothermic close relatives. The distribution of this character suggests that it co-evolved with red-muscle endothermy, hinting at a common physiological mechanism that would link bone histology to endothermy in these distantly related teleost lineages.
Keywords: Lampridiformes; Scombridae; Teleostei; bone histology; endothermy; osteocytes.
© 2018 The Author(s).
Conflict of interest statement
We have no competing interests.
Figures
(a–g)Lampris sp. (MNHN-ZA-AC-A-7506). Sections of the rib (natural transmitted light). (a) Entire cross section showing numerous vascular cavities (asterisks). (b) Longitudinal section showing numerous osteocyte lacunae. (c) Detail of inset 1 in (a), showing osteocyte lacunae (arrows) in primary bone. (d) Detail of inset 2 showing an area of primary bone with circularly-oriented osteocytes, and vascular cavities fringed by secondary bone. (e) Detail of an osteocyte (arrow) in primary bone with its radially-oriented canaliculi. (f) Longitudinal section showing osteocytes in primary bone. An osteocyte lacuna is seen in secondary bone (arrow). (g) Detail of inset 3 showing remodelled secondary bone including osteocytes without canaliculi (arrow). (h)Velifer hypselopterus (MNHN-ICOS-01117). Cross section of the scapula (transmitted natural light) showing the lack of osteocytes, but the presence of bifurcated (arrows) osteoblastic canaliculi inside the primary bony tissues. Some areas of secondary bone are visible. pb, primary bone; sb, secondary bone; vc, vascular cavity; *, marrow cavity. Arrowheads point to reversal lines between primary and secondary bone. Scale bars, (a) 500 µm, (b–d,g) 100 µm, (e–f,h) 50 µm.
Phylogenetic distribution of the osteohistological and metabolic parameters considered in this study among Neoteleostei. Acellular bone is in yellow, cellular bone in dark blue. Ectothermic taxa are in white, taxa with brain heaters (cranial-only endothermy) in light pink, with red-muscle endothermy in red. Tree topology is adapted from [1,15,17]. (Online version in colour.)
Similar articles
- The phylogenetic origin and evolution of acellular bone in teleost fishes: insights into osteocyte function in bone metabolism.Davesne D, Meunier FJ, Schmitt AD, Friedman M, Otero O, Benson RBJ.Davesne D, et al.Biol Rev Camb Philos Soc. 2019 Aug;94(4):1338-1363. doi: 10.1111/brv.12505. Epub 2019 Mar 28.Biol Rev Camb Philos Soc. 2019.PMID:30924235Review.
- Animal physiology. Whole-body endothermy in a mesopelagic fish, the opah, Lampris guttatus.Wegner NC, Snodgrass OE, Dewar H, Hyde JR.Wegner NC, et al.Science. 2015 May 15;348(6236):786-9. doi: 10.1126/science.aaa8902.Science. 2015.PMID:25977549
- Endothermy in the smalleye opah (Lampris incognitus): A potential role for the uncoupling protein sarcolipin.Franck JPC, Slight-Simcoe E, Wegner NC.Franck JPC, et al.Comp Biochem Physiol A Mol Integr Physiol. 2019 Jul;233:48-52. doi: 10.1016/j.cbpa.2019.03.024. Epub 2019 Apr 1.Comp Biochem Physiol A Mol Integr Physiol. 2019.PMID:30946978
- Evolution and consequences of endothermy in fishes.Dickson KA, Graham JB.Dickson KA, et al.Physiol Biochem Zool. 2004 Nov-Dec;77(6):998-1018. doi: 10.1086/423743.Physiol Biochem Zool. 2004.PMID:15674772Review.
- Evidence for cranial endothermy in the opah (Lampris guttatus).Runcie RM, Dewar H, Hawn DR, Frank LR, Dickson KA.Runcie RM, et al.J Exp Biol. 2009 Feb;212(Pt 4):461-70. doi: 10.1242/jeb.022814.J Exp Biol. 2009.PMID:19181893Free PMC article.
Cited by
- The evolution of mechanisms involved in vertebrate endothermy.Legendre LJ, Davesne D.Legendre LJ, et al.Philos Trans R Soc Lond B Biol Sci. 2020 Mar 2;375(1793):20190136. doi: 10.1098/rstb.2019.0136. Epub 2020 Jan 13.Philos Trans R Soc Lond B Biol Sci. 2020.PMID:31928191Free PMC article.Review.
- Mechanisms of dermal bone repair after predatory attack in the giant stem-group teleost Leedsichthys problematicus Woodward, 1889a (Pachycormiformes).Johanson Z, Liston J, Davesne D, Challands T, Meredith Smith M.Johanson Z, et al.J Anat. 2022 Aug;241(2):393-406. doi: 10.1111/joa.13689. Epub 2022 May 19.J Anat. 2022.PMID:35588137Free PMC article.
- Fossilized cell structures identify an ancient origin for the teleost whole-genome duplication.Davesne D, Friedman M, Schmitt AD, Fernandez V, Carnevale G, Ahlberg PE, Sanchez S, Benson RBJ.Davesne D, et al.Proc Natl Acad Sci U S A. 2021 Jul 27;118(30):e2101780118. doi: 10.1073/pnas.2101780118.Proc Natl Acad Sci U S A. 2021.PMID:34301898Free PMC article.
- Bone metabolism and evolutionary origin of osteocytes: Novel application of FIB-SEM tomography.Haridy Y, Osenberg M, Hilger A, Manke I, Davesne D, Witzmann F.Haridy Y, et al.Sci Adv. 2021 Mar 31;7(14):eabb9113. doi: 10.1126/sciadv.abb9113. Print 2021 Mar.Sci Adv. 2021.PMID:33789889Free PMC article.
References
Publication types
MeSH terms
Associated data
LinkOut - more resources
Full Text Sources
Other Literature Sources