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Scales and Tooth Whorls of Ancient Fishes Challenge Distinction between External and Oral 'Teeth'
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Evolution and Developmental Biology.
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Evolution and Developmental Biology.
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Evolution and Developmental Biology.
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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.

Place, publisher, year, edition, pages
2013. Vol. 8, no 8, e71890- p.
National Category
Natural Sciences
Identifiers
URN: urn:nbn:se:uu:diva-207634DOI: 10.1371/journal.pone.0071890ISI: 000323097300168OAI: oai:DiVA.org:uu-207634DiVA: diva2:649060
Available from: 2013-09-17 Created: 2013-09-17 Last updated: 2017-12-06Bibliographically approved
In thesis
1. Three-dimensional Virtual Histology of Early Vertebrate Scales Revealed by Synchrotron X-ray Phase-contrast Microtomography
Open this publication in new window or tab >>Three-dimensional Virtual Histology of Early Vertebrate Scales Revealed by Synchrotron X-ray Phase-contrast Microtomography
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
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:nbn:se:uu:diva-238056 (URN)978-91-554-9128-4 (ISBN)
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

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Qu, QingmingSanchez, SophieBlom, HenningAhlberg, Per Erik
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