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Development and three-dimensional histology of vertebrate dermal fin spines
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology. (Evolution and Development)
2016 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Jawed vertebrates (gnathostomes) consist of two clades with living representatives, the chondricthyans (cartilaginous fish including sharks, rays, and chimaeras) and the osteichthyans (bony fish and tetrapods), and two fossil groups, the "placoderms" and "acanthodians". These extinct forms were thought to be monophyletic, but are now considered to be paraphyletic partly due to the discovery of early chondrichthyans and osteichthyans with characters that had been previously used to define them. Among these are fin spines, large dermal structures that, when present, sit anterior to both median and/or paired fins in many extant and fossil jawed vertebrates. Making comparisons among early gnathostomes is difficult since the early chondrichthyans and "acanthodians", which have less mineralized skeleton, do not have large dermal bones on their skulls. As a result, fossil fin spines are potential sources for phylogenetic characters that could help in the study of the gnathostome evolutionary history. This thesis examines the development and internal structure of fin spines in jawed vertebrates using two-dimensional (2D) thin sections and three-dimensional (3D) synchrotron datasets. The development of the dorsal fin spine of the holocephalan, Callorhinchus milii, was described from embryos and compared to that of the neoselachian, Squalus acanthias, whose spine has been the model for studying fossil shark spines. It was found that the development of the C. milii fin presents differences from S. acanthias that suggest it might be a better candidate for studying "acanthodian" fin spines. The 3D histology of fossil fin spines was studied in Romundina stellina, a "placoderm"; Lophosteus superbus, a probable stem-osteichthyan; and sever­­al "acanthodians". The 3D vascularization reconstructed from synchrotron radiation microtomographic data reveal that "acanthodian" and Lophosteus spines grew similarly to what is observed in chondrichthyans, which differs slightly from the growth of the Romundina spine. Chondrichthyans and "acanthodians" also share similarities in their internal organization. Overall, Lophosteus and Romundina spines are more similar in terms of morphology and histology compared to chondrichthyans and "acanthodians". These results support the current hypothesis of gnathostome phylogeny, which places "acanthodians" on the chondrichthyan stem. They also emphasize the need for further study of vertebrate fin spines using 3D approaches.

Place, publisher, year, edition, pages
Uppsala: Acta Universitatis Upsaliensis, 2016. , 53 p.
Series
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology, ISSN 1651-6214 ; 1382
Keyword [en]
fin spine, paleontology, early vertebrate, histology, development
National Category
Natural Sciences Geosciences, Multidisciplinary
Research subject
Biology with specialization in Evolutionary Organismal Biology
Identifiers
URN: urn:nbn:se:uu:diva-286863ISBN: 978-91-554-9596-1 (print)OAI: oai:DiVA.org:uu-286863DiVA: diva2:922152
Public defence
2016-06-13, Lindahlsalen, Evolutionary Biology Center, Norbyvägen 18A, Uppsala, 09:00 (English)
Opponent
Supervisors
Available from: 2016-05-23 Created: 2016-04-21 Last updated: 2016-06-15
List of papers
1. Embryonic development of fin spines in Callorhinchus milii (Holocephali); implications for chondrichthyan fin spine evolution
Open this publication in new window or tab >>Embryonic development of fin spines in Callorhinchus milii (Holocephali); implications for chondrichthyan fin spine evolution
2014 (English)In: Evolution & Development, ISSN 1520-541X, E-ISSN 1525-142X, Vol. 16, no 6, 339-353 p.Article in journal (Refereed) Published
Abstract [en]

Fin spines are commonly known from fossil gnathostomes (jawed vertebrates) and are usually associated with paired and unpaired fins. They are less common among extant gnathostomes, being restricted to the median fins of certain chondrichthyans (cartilaginous fish), including chimaerids (elephant sharks) and neoselachians (sharks, skates, and rays). Fin spine growth is of great interest and relevance but few studies have considered their evolution and development. We investigated the development of the fin spine of the chimaerid Callorhinchus milii using stained histological sections from a series of larval, hatchling, and adult individuals. The lamellar trunk dentine of the Callorhinchus spine first condenses within the mesenchyme, rather than at the contact surface between mesenchyme and epithelium, in a manner more comparable to dermal bone formation than to normal odontode development. Trabecular dentine forms a small component of the spine under the keel; it is covered externally with a thin layer of lamellar trunk dentine, which is difficult to distinguish in sectioned adult spines. We suggest that the distinctive characteristics of the trunk dentine may reflect an origin through co-option of developmental processes involved in dermal bone formation. Comparison with extant Squalus and a range of fossil chondrichthyans shows that Callorhinchus is more representative than Squalus of generalized chondrichthyan fin-spine architecture, highlighting its value as a developmental model organism.

National Category
Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-240128 (URN)10.1111/ede.12104 (DOI)000345451100002 ()peahl255 (PubMedID)
Available from: 2015-01-08 Created: 2015-01-05 Last updated: 2017-12-05Bibliographically approved
2. Three-dimensional paleohistology of the scale and median fin spine of Lophosteus superbus (Pander 1856)
Open this publication in new window or tab >>Three-dimensional paleohistology of the scale and median fin spine of Lophosteus superbus (Pander 1856)
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2016 (English)In: PeerJ, ISSN 2167-8359, E-ISSN 2167-8359, Vol. 4, e2521Article in journal (Refereed) Published
Abstract [en]

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.

National Category
Natural Sciences
Research subject
Earth Science with specialization in Historical Geology and Palaeontology
Identifiers
urn:nbn:se:uu:diva-282529 (URN)10.7717/peerj.2521 (DOI)000387169900002 ()27833794 (PubMedID)
Funder
Swedish Research CouncilKnut and Alice Wallenberg FoundationEU, European Research Council, 233111
Available from: 2016-04-21 Created: 2016-04-05 Last updated: 2017-11-30Bibliographically approved
3. Vascularization and odontode structure of the median dorsal spine of Romundina stellina (Ørvig 1975)
Open this publication in new window or tab >>Vascularization and odontode structure of the median dorsal spine of Romundina stellina (Ørvig 1975)
Show others...
(English)Manuscript (preprint) (Other academic)
National Category
Natural Sciences
Identifiers
urn:nbn:se:uu:diva-282530 (URN)
Available from: 2016-04-21 Created: 2016-04-05 Last updated: 2016-06-15
4. Morphology and histology of 'acanthodian' fin spines from the Silurian Ramsåsa E locality, Skåne, Sweden
Open this publication in new window or tab >>Morphology and histology of 'acanthodian' fin spines from the Silurian Ramsåsa E locality, Skåne, Sweden
(English)Manuscript (preprint) (Other academic)
National Category
Natural Sciences
Identifiers
urn:nbn:se:uu:diva-286730 (URN)
Available from: 2016-04-21 Created: 2016-04-21 Last updated: 2016-06-15

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