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New genomic and fossil data illuminate the origin of enamel
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology. (Per Ahlberg)ORCID iD: 0000-0002-8291-8493
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Evolution and Developmental Biology.ORCID iD: 0000-0002-8754-5534
Institute of Vertebrate Paleontology and Paleoanthropology, Chinese Academy of Sciences.
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Evolution and Developmental Biology.
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.

Place, publisher, year, edition, pages
2015. Vol. 526, no 7571, 108-120 p.
National Category
Evolutionary Biology
Research subject
Biology
Identifiers
URN: urn:nbn:se:uu:diva-238055DOI: 10.1038/nature15259ISI: 000362095100043PubMedID: 26416752OAI: oai:DiVA.org:uu-238055DiVA: diva2:769966
Funder
Knut and Alice Wallenberg FoundationSwedish Research Council
Available from: 2014-12-09 Created: 2014-12-09 Last updated: 2017-12-05Bibliographically 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, QingmingHaitina, TatjanaAhlberg, Per Erik

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