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The Origin of Tooth Replacement: Three-dimensional Synchrotron Histology Visualizes the Dental Development of Silurian Stem Osteichthyans
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Organismal Biology, Evolution and Developmental Biology.
2017 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Mechanisms of tooth replacement distribute incongruently among extant gnathostomes (jawed vertebrates): a permanent tooth-generating dental lamina exists in chondrichthyans (cartilaginous fish) and tetrapods but not teleosts, whereas tooth shedding by basal hard tissue resorption occurs in tetrapods and teleosts but not chondrichthyans. Theories about the evolution of tooth development have been biased towards the chondrichthyan conveyor-belt replacement, since there has been no fossil evidence for the origin of osteichthyan (bony fish and tetrapods) tooth replacement until now. 3D virtual dissections with submicron-scale resolution, based on propagation phase contrast synchrotron microtomography (PPC-SRµCT), reveal the growth history of the dentitions of Andreolepis and Lophosteus, 423-Myr-old Silurian stem osteichthyans close to the common ancestor of tetrapods and teleosts. Their marginal jawbones and “tooth cushions” (possible homologues of coronoids) shed teeth by in situ cyclic basal resorption, the earliest examples of osteichthyan-style tooth replacement. The replacement cycles were site-autonomic, and occurred in broad irregular multi-row tooth fields, including at sites separated from the margin of the bone by intervening teeth, showing that the production of replacement teeth did not occur in a single deep dental lamina, but in pockets associated with each tooth, as in many teleosts. It suggests that the functionally and anatomically similar laminae of chondrichthyans and tetrapods are convergent. The marginal jaw bones of both genera carry an initial non-shedding dentition arranged in alternate transverse files, labial to the shedding tooth field, overgrown by later dermal ornament and probably not belonging to the oral domain, but bearing in vivo biting damage showing that they functioned as teeth. The most lingual of these odontodes have been resorbed apically and are overlain by shedding teeth. The first-generation teeth on the tooth cushions display basal resorption in Andreolepis, but semi-basal resorption in Lophosteus. The latter leaves a basal dentine ring from each tooth, implying only odontoclasts are involved in the semi-basal resorption, which is probably the first step towards evolving a site-specific resorption. The polarized displacement of each generation of resorption surfaces reflects the fact that the cyclic replacement, as well as the sequential addition of tooth sites, is closely related to bone growth. Resorption surfaces and growth arrest surfaces also record the life history and the replacement rate. These data provide unique insights into the origin of osteichthyan tooth replacement.

Place, publisher, year, edition, pages
Uppsala: Acta Universitatis Upsaliensis, 2017. , p. 53
Series
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology, ISSN 1651-6214 ; 1481
National Category
Evolutionary Biology
Identifiers
URN: urn:nbn:se:uu:diva-315885ISBN: 978-91-554-9829-0 (print)OAI: oai:DiVA.org:uu-315885DiVA, id: diva2:1076188
Public defence
2017-03-31, Lindahlsalen, Evolutionsbiologiskt centrum, Norbyvägen 14, Uppsala, 10:00 (English)
Opponent
Supervisors
Available from: 2017-03-10 Created: 2017-02-22 Last updated: 2017-03-20
List of papers
1. The stem osteichthyan Andreolepis and the origin of tooth replacement
Open this publication in new window or tab >>The stem osteichthyan Andreolepis and the origin of tooth replacement
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2016 (English)In: Nature, ISSN 0028-0836, E-ISSN 1476-4687, Vol. 539, no 7628, p. 237-+Article in journal (Refereed) Published
Abstract [en]

The teeth of gnathostomes (jawed vertebrates) show rigidly patterned, unidirectional replacement that may or may not be associated with a shedding mechanism. These mechanisms, which are critical for the maintenance of the dentition, are incongruently distributed among extant gnathostomes. Although a permanent tooth-generating dental lamina is present in all chondrichthyans, many tetrapods and some teleosts, it is absent in the non-teleost actinopterygians. Tooth-shedding by basal hard tissue resorption occurs in most osteichthyans (including tetrapods) but not in chondrichthyans. Here we report a three-dimensional virtual dissection of the dentition of a 424-million-year-old stem osteichthyan, Andreolepis hedei, using propagation phase-contrast synchrotron microtomography, with a reconstruction of its growth history. Andreolepis, close to the common ancestor of all extant osteichthyans, shed its teeth by basal resorption but probably lacked a permanent dental lamina. This is the earliest documented instance of resorptive tooth shedding and may represent the primitive osteichthyan mode of tooth replacement.

National Category
Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-310754 (URN)10.1038/nature19812 (DOI)000387318500034 ()27750278 (PubMedID)
Funder
EU, European Research Council, 233111Knut and Alice Wallenberg Foundation
Available from: 2016-12-20 Created: 2016-12-19 Last updated: 2017-11-29Bibliographically approved
2. Development of cyclic shedding teeth from semi-shedding teeth: the inner dental arcade of the stem osteichthyan Lophosteus 
Open this publication in new window or tab >>Development of cyclic shedding teeth from semi-shedding teeth: the inner dental arcade of the stem osteichthyan Lophosteus 
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2017 (English)In: Royal Society Open Science, E-ISSN 2054-5703, Vol. 4, no 5, article id 161084Article in journal (Refereed) Published
Abstract [en]

The numerous cushion-shaped tooth-bearing plates attributed to the stem-group osteichthyan Lophosteus superbus, which are argued here to represent the ancient form of inner dental arcade, display a unique and presumably primitive way of tooth shedding by basal hard tissue resorption. They carry regularly spaced, recumbent, gently recurved teeth arranged in transverse tooth files that diverge towards the lingual margin of the cushion. Three-dimensional (3D) reconstruction from propagation phase contrast synchrotron microtomography (PPC-SRμCT) reveals remnants of the first-generation teeth embedded in the basal plate that have never been discerned in any taxa. These teeth were shed by semi-basal resorption with the periphery of their bases retained as dentine rings. The rings are highly overlapped, which evidences tooth shedding prior to adding the next first-generation tooth. Later teeth at the same sites underwent cyclical replacing and shedding through basal resorption, producing stacks of buried resorption surfaces separated by bone of attachment. The number and spatial arrangement of resorption surfaces elucidates that basal resorption of replacement teeth had taken place at the older tooth sites before the addition of the youngest first-generation teeth at the lingual margin. Thus the replacement tooth buds cannot have been generated by a single permanent dental lamina, but must have arisen either from successional dental laminae associated with the predecessor teeth, or directly from the dental epithelium of these teeth. The virtual histological dissection of these Late Silurian microfossils broadens our understanding of the development of the gnathostome dental systems and the acquisition of the osteichthyan-type of tooth replacement. 

Place, publisher, year, edition, pages
ROYAL SOC, 2017
National Category
Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-315882 (URN)10.1098/rsos.161084 (DOI)000402541800020 ()28573003 (PubMedID)
Available from: 2017-02-22 Created: 2017-02-22 Last updated: 2017-08-02Bibliographically approved
3. Microstructures of the most primitive form of inner dental arcade and life history of the Silurian stem osteichthyan Andreolepis.
Open this publication in new window or tab >>Microstructures of the most primitive form of inner dental arcade and life history of the Silurian stem osteichthyan Andreolepis.
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(English)Manuscript (preprint) (Other academic)
National Category
Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-315883 (URN)
Available from: 2017-02-22 Created: 2017-02-22 Last updated: 2017-02-22
4. The marginal dentition of Lophosteus superbus Pander 1856, a Late Silurian stem osteichthyan from Estonia.
Open this publication in new window or tab >>The marginal dentition of Lophosteus superbus Pander 1856, a Late Silurian stem osteichthyan from Estonia.
(English)Manuscript (preprint) (Other academic)
National Category
Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-315884 (URN)
Available from: 2017-02-22 Created: 2017-02-22 Last updated: 2017-02-22

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