journal article
Open Access
Nov 02, 2016
Three-dimensional paleohistology of the scale and median fin spine of Lophosteus superbus (Pander 1856)
Abstract
Lophosteus superbus
is one of only a handful of probable stem-group osteichthyans known from the fossil record. First collected and described in the late 19th century from the upper Silurian Saaremaa Cliff locality in Estonia, it is known from a wealth of disarticulated scales, fin spines, and bone fragments. In this study we provide the first description of the morphology and paleohistology of a fin spine and scale from
Lophosteus
using virtual thin sections and 3D reconstructions that were segmented using phase-contrast synchrotron X-ray microtomography. These data reveal that both structures have fully or partially buried odontodes, which retain fine morphological details in older generations, including sharp nodes and serrated ridgelets. The vascular architecture of the fin spine tip, which is composed of several layers of longitudinally directed bone vascular canals, is much more complex compared to the bulbous horizontal canals within the scale, but they both have distinctive networks of ascending canals within each individual odontode. Other histological characteristics that can be observed from the data are cell spaces and Sharpey’s fibers that, when combined with the vascularization, could help to provide insights into the growth of the structure. The 3D data of the scales from
Lophosteus superbus
is similar to comparable data from other fossil osteichthyans, and the morphology of the reconstructed buried odontodes from this species is identical to scale material of
Lophosteus ohesaarensis
, casting doubt on the validity of that species. The 3D data presented in this paper is the first for fossil fin spines and so comparable data is not yet available. However, the overall morphology and histology seems to be similar to the structure of placoderm dermal plates. The 3D datasets presented here provide show that microtomography is a powerful tool for investigating the three-dimensional microstructure of fossils, which is difficult to study using traditional histological methods. These results also increase the utility of fin spines and scales suggest that these data are a potentially rich source of morphological data that could be used for studying questions relating to early vertebrate growth and evolution.
is one of only a handful of probable stem-group osteichthyans known from the fossil record. First collected and described in the late 19th century from the upper Silurian Saaremaa Cliff locality in Estonia, it is known from a wealth of disarticulated scales, fin spines, and bone fragments. In this study we provide the first description of the morphology and paleohistology of a fin spine and scale from
Lophosteus
using virtual thin sections and 3D reconstructions that were segmented using phase-contrast synchrotron X-ray microtomography. These data reveal that both structures have fully or partially buried odontodes, which retain fine morphological details in older generations, including sharp nodes and serrated ridgelets. The vascular architecture of the fin spine tip, which is composed of several layers of longitudinally directed bone vascular canals, is much more complex compared to the bulbous horizontal canals within the scale, but they both have distinctive networks of ascending canals within each individual odontode. Other histological characteristics that can be observed from the data are cell spaces and Sharpey’s fibers that, when combined with the vascularization, could help to provide insights into the growth of the structure. The 3D data of the scales from
Lophosteus superbus
is similar to comparable data from other fossil osteichthyans, and the morphology of the reconstructed buried odontodes from this species is identical to scale material of
Lophosteus ohesaarensis
, casting doubt on the validity of that species. The 3D data presented in this paper is the first for fossil fin spines and so comparable data is not yet available. However, the overall morphology and histology seems to be similar to the structure of placoderm dermal plates. The 3D datasets presented here provide show that microtomography is a powerful tool for investigating the three-dimensional microstructure of fossils, which is difficult to study using traditional histological methods. These results also increase the utility of fin spines and scales suggest that these data are a potentially rich source of morphological data that could be used for studying questions relating to early vertebrate growth and evolution.
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References
56
[1]
Ahlberg "Osteology and morphology of the probable stem-group osteichthyan Lophosteus superbus Pander, from the Silurian of Estonia" (2013)
[2]
Basden "A primitive actinopterygian neurocranium from the Early Devonian of southeastern Australia" Journal of Vertebrate Paleontology (2001) 10.1671/0272-4634(2001)021[0754:apanft]2.0.co;2
[3]
Botella "Jaws and teeth of the earliest bony fishes" Nature (2007) 10.1038/nature05989
[4]
Brazeau "The braincase and jaws of a Devonian ‘acanthodian’ and modern gnathostome origins" Nature (2009) 10.1038/nature07436
[5]
Brazeau "The characters of Palaeozoic jawed vertebrates" Zoological Journal of the Linnean Society (2014) 10.1111/zoj.12111
[6]
Burrow "A new lophosteiform (Osteichthyes) from the Lower Devonian of Australia" Geobios Memoire Special (1995) 10.1016/s0016-6995(95)80134-0
[7]
Burrow "Revision of Climatius reticulatus Agassiz, 1844 (Acanthodii, Climatiidae), from the Lower Devonian of Scotland, based on new histological and morphological data" Journal of Vertebrate Paleontology (2015) 10.1080/02724634.2014.913421
[8]
Burrow "The diplacanthid fishes (Acanthodii, Diplacanthiformes, Diplacanthidae) from the Middle Devonian of Scotland" Palaeontologia Electronica (2016)
[9]
Burrow "A new look at Machaeracanthus" (2010)
[10]
Burrow "Redescription of Parexus recurvus, an Early Devonian acanthodian from the Midland Valley of Scotland" Alcheringa: an Australasian Journal of Palaeontology (2013) 10.1080/03115518.2013.765656
[11]
Burrow "A review of placoderm scales ad their significance in placoderm phylogeny" Journal of Vertebrate Paleontology (1999) 10.1080/02724634.1999.10011135
[12]
Chen "Scale morphology and squamation of the Late Silurian osteichthyan Andreolepis from Gotland, Sweden" Historical Biology (2012) 10.1080/08912963.2012.668187
[13]
Cunningham "Testing models of dental development in the earliest bony vertebrates, Andreolepis and Lophosteus" Biology Letters (2012) 10.1098/rsbl.2012.0357
[14]
Denison "Acanthodii" (1979)
[15]
Dupret "A primitive placoderm sheds light on the origin of the jawed vertebrate face" Nature (2014) 10.1038/nature12980
[16]
Francillon-Vieillot "Microstructure and mineralization of vertebrate skeletal tissues" (1990)
[17]
Giles "Osteichthyan-like cranial conditions in an Early Devonian stem gnathostome" Nature (2015) 10.1038/nature14065
[18]
Giles "Histology of “Placoderm” dermal skeletons: implications for the nature of the ancestral gnathostome" Journal of Morphology (2013) 10.1002/jmor.20119
[19]
Gross "Lophosteus superbus Pander, ein ‘Teleostome aus dem Silur Oesels" Lethaia (1969) 10.1111/j.1502-3931.1969.tb01249.x
[20]
Gross "Lophosteus superbus Pander: Zaehne, Zahnknochen und besondere Schuppenformen" Lethaia (1971) 10.1111/j.1502-3931.1971.tb01285.x
[21]
Janvier "On the oldest known teleostome fish Andreolepis hedei Gross (Ludlow of Gotland), and the systematic position of the lophosteids" Eesti NSV Teaduste Akadeemia toimetised Geoloogia (1978)
[22]
Janvier (1996) 10.1093/oso/9780198540472.001.0001
[23]
Jerve "Embryonic development of fin spines in Callorhinchus milii (Holocephali); implications for chondrichthyan fin spine evolution" Evolution and Development (2014) 10.1111/ede.12104
[24]
Jessen "Moythomasia nitida Gross und M. cf. striata Gross, Devonische Palaeonisciden aus dem oberen Plattenkalk der Bergisch-Gladbach—Paffrather Mulde (Rheinisches Schiefergebirge)" Palaeontographica Abteilung A (1968)
[25]
Labiche "The fast readout low noise camera as a versatile X-ray detector for time resolved dispersive extended X-ray absorption fine structure and diffraction studies of dynamic problems in materials science, chemistry, and catalysis" Review of Scientific Instruments (2007) 10.1063/1.2783112
[26]
Maisey "Fin spine morphogenesis in squalid and heterodontid sharks" Zoological Journal of Linnaean Society (1979) 10.1111/j.1096-3642.1979.tb01907.x
[27]
Märss "Silurian vertebrates of Estonia and West Latvia" Fossilia Baltica (1986)
[28]
Märss "Vertebrates of the Pridoli and Silurian–Devonian boundary beds in Europe" Modern Geology (1997)
[29]
Märss "Distribution of Silurian and Lower Devonian vertebrate microremains and conodonts in the Baillie-Hamilton and Cornwallis Island sections, Canadian Arctic" Proceedings of the Estonian Academy of Sciences, Geology (1998) 10.3176/geol.1998.2.01
[30]
Martin "LSO-based single crystal film scintillator for synchrotron-based hard X-ray micro-imaging" IEEE Transactions on Nuclear Science (2009) 10.1109/tns.2009.2015878
[31]
Miles "Relationships of acanthodians. 63–103" (1973)
[32]
Ørvig "Histologic studies of Placoderms and fossil Elasmobranchs. I: the endoskeleton, with remarks on the hard tissues of lower vertebrates in general" Arkiv för Zoologi (1951)
[33]
Ørvig "Description, with special reference to the dermal skeleton, of a new radotinid arthrodire from the Gedinnian of Arctic Canada" (1975)
[34]
Ørvig "A survey of odontodes (“dermal teeth”) from developmental, structural, functional, and phyletic points of view" (1977)
[35]
Otto "Zur systematischen Stellung der Lophosteiden (Obersilur, Pisces inc. sedis)" Paläontologische Zeitschrift (1991) 10.1007/bf02989850
[36]
Pander (1856)
[37]
Qu "Three-dimensional virtual histology of Silurian osteostracan scales revealed by synchrotron radiation microtomography" Journal of Morphology (2015) 10.1002/jmor.20386
[38]
Qu "Genomic and fossil data illuminate the origin of enamel" Nature (2015) 10.1038/nature15259
[39]
Qu "Scales and tooth whorls of ancient fishes challenge distinction between external and oral ‘teeth’" PLoS ONE (2013) 10.1371/journal.pone.0071890
[40]
Qu "The origin of novel features by changes in developmental mechanisms: ontogeny and three-dimensional microanatomy of polyodontode scales of two early osteichthyans" Biological Reviews (2016) 10.1111/brv.12277
[41]
Qu "Scales and dermal skeletal histology of an early bony fish Psarolepis romeri and their bearing on the evolution of rhombic scales and hard tissue" PLoS ONE (2013) 10.1371/journal.pone.0061485
[42]
Rohon "Die Obersiluischen Fische von Oesel. Theil 2" Mémoires de l’Académie Impériale des Sciences de St. Pétersbourg (1893)
[43]
Rücklin "Romundina and the evolutionary origin of teeth" Biology Letters (2015) 10.1098/rsbl.2015.0326
[44]
Sanchez "Three-dimensional synchrotron virtual paleohistology: a new insight into the world of fossil bone microstructures" Microscopy and Microanalysis (2012) 10.1017/s1431927612001079
[45]
Schultze "Scales, enamel, cosmine, ganoine, and early osteichthyans" Comptes Rendus Palevol (2015) 10.1016/j.crpv.2015.04.001
[46]
Schultze "Dialipina and the characters of basal actinopterygians" (2001)
[47]
Schultze "Revisiting Lophosteus Pander, 1856, a primitive osteichthyan" Acta Universitatis Latviensis (2004)
[48]
Soler-Gijón "Occipital spine of Orthacanthus (Xenacanthidae, Elasmobranchii): structure and growth" Journal of Morphology (1999) 10.1002/(sici)1097-4687(199910)242:1<1::aid-jmor2>3.0.co;2-9
[49]
Trinajstic "Scale morphology of the Late Devonian palaeoniscoid Moythomasia durgaringa Gardiner and Bartram, 1997" Alcheringa (1999) 10.1080/03115519908619335
[50]
Valiukevičius "Diversity of tissues in acanthodians with Nostolepis- type histological structure" Acta Palaeontologica Polonica (2005)
Showing 50 of 56 references
Metrics
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Citations
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References
Details
- Published
- Nov 02, 2016
- Vol/Issue
- 4
- Pages
- e2521
- License
- View
Authors
Funding
Vetenskapsrådet
Swedish Research council
ERC Advanced Investigator Grant
Award: 233111
Knut and Alice Wallenberg Foundation
European Synchrotron Radiation Facility proposal EC 688
Cite This Article
Anna Jerve, Qingming Qu, Sophie Sanchez, et al. (2016). Three-dimensional paleohistology of the scale and median fin spine of
Lophosteus superbus
(Pander 1856). PeerJ, 4, e2521. https://doi.org/10.7717/peerj.2521
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