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Three-dimensional Virtual Histology of Early Vertebrate Scales Revealed by Synchrotron X-ray Phase-contrast Microtomography
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology. (Per Ahlberg)ORCID iD: 0000-0002-8291-8493
2015 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Vertebrate hard tissues first appeared in the dermal skeletons of early jawless vertebrates (ostracoderms) and were further modified in the earliest jawed vertebrates. Fortunately, histological information is usually preserved in these early vertebrate fossils and has thus been studied for more than a century, done so by examining thin sections, which provide general information about the specific features of vertebrate hard tissues in their earliest forms. Recent progress in synchrotron X-ray microtomography technology has caused a revolution in imaging methods used to study the dermal skeletons of early vertebrates. Virtual thin sections obtained in this manner can be used to reconstruct the internal structures of dermal skeletons in three-dimensions (3D), such as vasculature, buried odontodes (tooth-like unites) and osteocytes. Several body scales of early vertebrates have been examined using this imaging method and in situ 3D models of internal structures are created. Andreolepis (an early osteichthyan) scale shows linear growth pattern of odontodes in early developmental stage, which is not observable in traditional thin sections. The scale of another early osteichthyan Psarolepis was studied in the same way. Comparison between Andreolepis and Psarolepis shows that cosmine, a tissue complex in dermal skeleton of early sarcopterygians, originated by a developmental change of odontode shape. Two scales of osteostracans, a group of extinct jawless vertebrates, were studied in 3D and more details have been revealed in comparison to previous results based solely on 2D thin sections. 3D data enables us to compare the vasculature and canal system in different taxa in great detail, which forms the basis of formulating primary homology hypothesis and phylogenetic characters.

The new data resulting from this study suggests that vertebrate fossils have preserved much more histological information than we currently appreciate, and provide a new data source of microanatomical structures inside the fossils that can contribute new characters for phylogenetic analysis of early jawed vertebrates.

Place, publisher, year, edition, pages
Uppsala: Acta Universitatis Upsaliensis, 2015. , 49 p.
Series
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology, ISSN 1651-6214 ; 1213
Keyword [en]
3D virtual paleohistology, scales, ontogeny, jawed vertebrates, phylogeny
National Category
Evolutionary Biology
Research subject
Biology; Earth Science with specialization in Historical Geology and Palaeontology
Identifiers
URN: urn:nbn:se:uu:diva-238056ISBN: 978-91-554-9128-4 (print)OAI: oai:DiVA.org:uu-238056DiVA: diva2:770409
Public defence
2015-02-02, Lindahlsalen, Norbyvägen 18A, Uppsala, 14:00 (English)
Opponent
Supervisors
Funder
EU, European Research Council, 233111
Available from: 2015-01-09 Created: 2014-12-09 Last updated: 2015-02-03Bibliographically approved
List of papers
1. Scales and Dermal Skeletal Histology of an Early Bony Fish Psarolepis romeri and Their Bearing on the Evolution of Rhombic Scales and Hard Tissues
Open this publication in new window or tab >>Scales and Dermal Skeletal Histology of an Early Bony Fish Psarolepis romeri and Their Bearing on the Evolution of Rhombic Scales and Hard Tissues
2013 (English)In: PLoS ONE, ISSN 1932-6203, E-ISSN 1932-6203, Vol. 8, no 4, e61485- p.Article in journal (Refereed) Published
Abstract [en]

Recent discoveries of early bony fishes from the Silurian and earliest Devonian of South China (e. g. Psarolepis, Achoania, Meemannia, Styloichthys and Guiyu) have been crucial in understanding the origin and early diversification of the osteichthyans (bony fishes and tetrapods). All these early fishes, except Guiyu, have their dermal skeletal surface punctured by relatively large pore openings. However, among these early fishes little is known about scale morphology and dermal skeletal histology. Here we report new data about the scales and dermal skeletal histology of Psarolepis romeri, a taxon with important implications for studying the phylogeny of early gnathostomes and early osteichthyans. Seven subtypes of rhombic scales with similar histological composition and surface sculpture are referred to Psarolepis romeri. They are generally thick and show a faint antero-dorsal process and a broad peg-and-socket structure. In contrast to previously reported rhombic scales of osteichthyans, these scales bear a neck between crown and base as in acanthodian scales. Histologically, the crown is composed of several generations of odontodes and an irregular canal system connecting cylindrical pore cavities. Younger odontodes are deposited on older ones both superpositionally and areally. The bony tissues forming the keel of the scale are shown to be lamellar bone with plywood-like structure, whereas the other parts of the base are composed of pseudo-lamellar bone with parallel collagen fibers. The unique tissue combination in the keel (i.e., extrinsic Sharpey's fibers orthogonal to the intrinsic orthogonal sets of collagen fibers) has rarely been reported in the keel of other rhombic scales. The new data provide insights into the early evolution of rhombic (ganoid and cosmoid) scales in osteichthyans, and add to our knowledge of hard tissues of early vertebrates.

National Category
Natural Sciences
Identifiers
urn:nbn:se:uu:diva-200692 (URN)10.1371/journal.pone.0061485 (DOI)000317909600117 ()
Available from: 2013-06-03 Created: 2013-06-03 Last updated: 2017-12-06Bibliographically approved
2. Scales and Tooth Whorls of Ancient Fishes Challenge Distinction between External and Oral 'Teeth'
Open this publication in new window or tab >>Scales and Tooth Whorls of Ancient Fishes Challenge Distinction between External and Oral 'Teeth'
Show others...
2013 (English)In: PLoS ONE, ISSN 1932-6203, E-ISSN 1932-6203, Vol. 8, no 8, e71890- p.Article in journal (Refereed) Published
Abstract [en]

The debate about the origin of the vertebrate dentition has been given fresh fuel by new fossil discoveries and developmental studies of extant animals. Odontodes (teeth or tooth-like structures) can be found in two distinct regions, the 'internal' oropharyngeal cavity and the 'external' skin. A recent hypothesis argues that regularly patterned odontodes is a specific oropharyngeal feature, whereas odontodes in the external skeleton lack this organization. However, this argument relies on the skeletal system of modern chondrichthyans (sharks and their relatives), which differ from other gnathostome (jawed vertebrate) groups in not having dermal bones associated with the odontodes. Their external skeleton is also composed of monoodontode 'placoid scales', whereas the scales of most early fossil gnathostomes are polyodontode, i.e. constructed from several odontodes on a shared bony base. Propagation phase contrast X-ray Synchrotron microtomography (PPC-SRmCT) is used to study the polyodontode scales of the early bony fish Andreolepis hedei. The odontodes constructing a single scale are reconstructed in 3D, and a linear and regular growth mechanism similar to that in a gnathostome dentition is confirmed, together with a second, gap-filling growth mechanism. Acanthodian tooth whorls are described, which show that ossification of the whorl base preceded and probably patterned the development of the dental lamina, in contrast to the condition in sharks where the dental lamina develops early and patterns the dentition. The new findings reveal, for the first time, how polyodontode scales grow in 3D in an extinct bony fish. They show that dentition-like odontode patterning occurs on scales and that the primary patterning unit of a tooth whorl may be the bony base rather than the odontodes it carries. These results contradict the hypothesis that oropharyngeal and external odontode skeletons are fundamentally separate and suggest that the importance of dermal bone interactions to odontode patterning has been underestimated.

National Category
Natural Sciences
Identifiers
urn:nbn:se:uu:diva-207634 (URN)10.1371/journal.pone.0071890 (DOI)000323097300168 ()
Available from: 2013-09-17 Created: 2013-09-17 Last updated: 2017-12-06Bibliographically approved
3. The origin of novel features by changes in developmental mechanisms: a 3D virtual paleohistology study on polyodontode scales of primitive osteichthyans
Open this publication in new window or tab >>The origin of novel features by changes in developmental mechanisms: a 3D virtual paleohistology study on polyodontode scales of primitive osteichthyans
Show others...
2015 (English)Manuscript (preprint) (Other academic)
Keyword
3D paleohistology, origin of cosmine, odontode, ontogeny, phylogeny
National Category
Evolutionary Biology
Research subject
Earth Science with specialization in Historical Geology and Palaeontology
Identifiers
urn:nbn:se:uu:diva-237343 (URN)
Funder
EU, European Research Council, 233111
Available from: 2014-12-09 Created: 2014-12-01 Last updated: 2017-06-30Bibliographically approved
4. Three-dimensional virtual histology of silurian osteostracan scales revealed by synchrotron radiation microtomography
Open this publication in new window or tab >>Three-dimensional virtual histology of silurian osteostracan scales revealed by synchrotron radiation microtomography
2015 (English)In: Journal of morphology (1931. Print), ISSN 0362-2525, E-ISSN 1097-4687, Vol. 276, no 8, 873-888 p.Article in journal (Refereed) Published
National Category
Evolutionary Biology
Research subject
Earth Science with specialization in Historical Geology and Palaeontology
Identifiers
urn:nbn:se:uu:diva-238054 (URN)10.1002/jmor.20386 (DOI)000358371700001 ()
Funder
EU, European Research Council, 233111Knut and Alice Wallenberg Foundation
Available from: 2014-12-09 Created: 2014-12-09 Last updated: 2017-12-05Bibliographically approved
5. New genomic and fossil data illuminate the origin of enamel
Open this publication in new window or tab >>New genomic and fossil data illuminate the origin of enamel
2015 (English)In: Nature, ISSN 0028-0836, E-ISSN 1476-4687, Vol. 526, no 7571, 108-120 p.Article in journal, Letter (Refereed) Published
Abstract [en]

Enamel, the hardest vertebrate tissue, covers the teeth of almost all sarcopterygians (lobe-finned bony fishes and tetrapods) as well as the scales and dermal bones of many fossil lobe-fins(1-5). Enamel deposition requires an organic matrix containing the unique enamel matrix proteins (EMPs) amelogenin (AMEL), enamelin (ENAM) and ameloblastin (AMBN)(6). Chondrichthyans (cartilaginous fishes) lack both enamel and EMP genes(7,8). Many fossil and a few living non-teleost actinopterygians (ray-finned bony fishes) such as the gar, Lepisosteus, have scales and dermal bones covered with a proposed enamel homologue called ganoine(1,9). However, no gene or transcript data for EMPs have been described from actinopterygians(10,11). Here we show that Psarolepis romeri, a bony fish from the the Early Devonian period, combines enamel-covered dermal odontodes on scales and skull bones with teeth of naked dentine, and that Lepisosteus oculatus (the spotted gar) has enam andambn genes that are expressed in the skin, probably associated with ganoine formation. The genetic evidence strengthens the hypothesis that ganoine is homologous with enamel. The fossil evidence, further supported by the Silurian bony fish Andreolepis, which has enamel-covered scales but teeth and odontodes on its dermal bones made of naked dentine(12-16), indicates that this tissue originated on the dermal skeleton, probably on the scales. It subsequently underwent heterotopic expansion across two highly conserved patterning boundaries (scales/head-shoulder and dermal/oral) within the odontode skeleton.

National Category
Evolutionary Biology
Research subject
Biology
Identifiers
urn:nbn:se:uu:diva-238055 (URN)10.1038/nature15259 (DOI)000362095100043 ()26416752 (PubMedID)
Funder
Knut and Alice Wallenberg FoundationSwedish Research Council
Available from: 2014-12-09 Created: 2014-12-09 Last updated: 2017-12-05Bibliographically approved

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