Acanthodian dental development and the origin of gnathostome dentitions

Martin Rucklin; Benedict King; John A Cunningham; Zerina Johanson; Federica Marone; Philip C J Donoghue

doi:10.1038/s41559-021-01458-4

Acanthodian dental development and the origin of gnathostome dentitions

Martin Rucklin^*, Benedict King, John A Cunningham, Zerina Johanson, Federica Marone, Philip C J Donoghue ^*

^*Corresponding author for this work

Research output: Contribution to journal › Article (Academic Journal) › peer-review

14 Citations (Scopus)

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Abstract

Chondrichthyan dentitions are conventionally interpreted to reflect the ancestral gnathostome condition but interpretations of osteichthyan dental evolution in this light have proven unsuccessful, perhaps because chondrichthyan dentitions are equally specialized, or else independently evolved. Ischnacanthid acanthodians are stem-Chondrichthyes; as phylogenetic intermediates of osteichthyans and crown chondrichthyans, the nature of their enigmatic dentition may inform homology and the ancestral gnathostome condition. Here we show that ischnacanthid marginal dentitions were statodont, composed of multicuspidate teeth added in distally diverging rows and through proximal superpositional replacement, while their symphyseal tooth whorls are comparable to chondrichthyan and osteichthyan counterparts. Ancestral state estimation indicates the presence of oral tubercles on the jaws of the gnathostome crown-ancestor; tooth whorls and/or tooth rows evolved independently in placoderms, osteichthyans, ischnacanthids, other acanthodians and crown-chondrichthyans. Crown-chondrichthyan dentitions are derived relative to the gnathostome crown-ancestor which possessed a simple dentition and lacked a permanent dental lamina which evolved independently in Chondrichthyes and Osteichthyes.

Original language	English
Pages (from-to)	919-926
Number of pages	8
Journal	Nature Ecology and Evolution
Volume	5
Issue number	7
Early online date	6 May 2021
DOIs	https://doi.org/10.1038/s41559-021-01458-4
Publication status	Published - Jul 2021

Bibliographical note

Funding Information:
We thank S. Bengtson and D. Murdock for help at the TOMCAT beamline. We also thank E. Bernard (Natural History Museum) for access to collections and for facilitating the loan of specimens. The study was funded by an EU FP7 Marie-Curie Intra-European Fellowship (to M.R. and P.C.J.D.), Natural Environmental Research Council grant NE/G016623/1 (to P.C.J.D.) and Nederlandse Organisatie voor Wetenschappelijk Onderzoek (NWO) (VIDI 864.14.009 to M.R.). We acknowledge the Paul Scherrer Institut, Villigen, Switzerland, for provision of synchrotron radiation beamtime at the TOMCAT (X02DA) beamline of the Swiss Light Source (to P.C.J.D. and S. Bengtson).

Publisher Copyright:
© 2021, The Author(s), under exclusive licence to Springer Nature Limited.

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This is the author accepted manuscript (AAM). The final published version (version of record) is available online via Nature Research at https://doi.org/10.1038/s41559-021-01458-4 . Please refer to any applicable terms of use of the publisher.
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Teeth and jaws: evolutionary emergence of a model organogenic system and the adaptive radiation of gnathosomes.
Donoghue, P. C. J. (Principal Investigator)
1/10/09 → 1/10/13
Project: Research

Data from Rücklin et al. 2021. Acanthodian dental development and the origin of gnathostome dentitions. Nature Ecology & Evolution
Rücklin, M. (Creator), King, B. (Creator), Cunningham, J. A. (Creator), Johanson, Z. (Creator), Marone, F. (Creator) & Donoghue, P. (Contributor), University of Bristol, 29 Mar 2021
DOI: 10.5523/bris.1557rzkyzst5b2jagjuz9li5er, http://data.bris.ac.uk/data/dataset/1557rzkyzst5b2jagjuz9li5er
Dataset

Cite this

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title = "Acanthodian dental development and the origin of gnathostome dentitions",

abstract = "Chondrichthyan dentitions are conventionally interpreted to reflect the ancestral gnathostome condition but interpretations of osteichthyan dental evolution in this light have proven unsuccessful, perhaps because chondrichthyan dentitions are equally specialized, or else independently evolved. Ischnacanthid acanthodians are stem-Chondrichthyes; as phylogenetic intermediates of osteichthyans and crown chondrichthyans, the nature of their enigmatic dentition may inform homology and the ancestral gnathostome condition. Here we show that ischnacanthid marginal dentitions were statodont, composed of multicuspidate teeth added in distally diverging rows and through proximal superpositional replacement, while their symphyseal tooth whorls are comparable to chondrichthyan and osteichthyan counterparts. Ancestral state estimation indicates the presence of oral tubercles on the jaws of the gnathostome crown-ancestor; tooth whorls and/or tooth rows evolved independently in placoderms, osteichthyans, ischnacanthids, other acanthodians and crown-chondrichthyans. Crown-chondrichthyan dentitions are derived relative to the gnathostome crown-ancestor which possessed a simple dentition and lacked a permanent dental lamina which evolved independently in Chondrichthyes and Osteichthyes.",

author = "Martin Rucklin and Benedict King and Cunningham, {John A} and Zerina Johanson and Federica Marone and Donoghue, {Philip C J}",

note = "Funding Information: We thank S. Bengtson and D. Murdock for help at the TOMCAT beamline. We also thank E. Bernard (Natural History Museum) for access to collections and for facilitating the loan of specimens. The study was funded by an EU FP7 Marie-Curie Intra-European Fellowship (to M.R. and P.C.J.D.), Natural Environmental Research Council grant NE/G016623/1 (to P.C.J.D.) and Nederlandse Organisatie voor Wetenschappelijk Onderzoek (NWO) (VIDI 864.14.009 to M.R.). We acknowledge the Paul Scherrer Institut, Villigen, Switzerland, for provision of synchrotron radiation beamtime at the TOMCAT (X02DA) beamline of the Swiss Light Source (to P.C.J.D. and S. Bengtson). Publisher Copyright: {\textcopyright} 2021, The Author(s), under exclusive licence to Springer Nature Limited.",

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AU - King, Benedict

AU - Cunningham, John A

AU - Johanson, Zerina

AU - Marone, Federica

AU - Donoghue , Philip C J

N1 - Funding Information: We thank S. Bengtson and D. Murdock for help at the TOMCAT beamline. We also thank E. Bernard (Natural History Museum) for access to collections and for facilitating the loan of specimens. The study was funded by an EU FP7 Marie-Curie Intra-European Fellowship (to M.R. and P.C.J.D.), Natural Environmental Research Council grant NE/G016623/1 (to P.C.J.D.) and Nederlandse Organisatie voor Wetenschappelijk Onderzoek (NWO) (VIDI 864.14.009 to M.R.). We acknowledge the Paul Scherrer Institut, Villigen, Switzerland, for provision of synchrotron radiation beamtime at the TOMCAT (X02DA) beamline of the Swiss Light Source (to P.C.J.D. and S. Bengtson). Publisher Copyright: © 2021, The Author(s), under exclusive licence to Springer Nature Limited.

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N2 - Chondrichthyan dentitions are conventionally interpreted to reflect the ancestral gnathostome condition but interpretations of osteichthyan dental evolution in this light have proven unsuccessful, perhaps because chondrichthyan dentitions are equally specialized, or else independently evolved. Ischnacanthid acanthodians are stem-Chondrichthyes; as phylogenetic intermediates of osteichthyans and crown chondrichthyans, the nature of their enigmatic dentition may inform homology and the ancestral gnathostome condition. Here we show that ischnacanthid marginal dentitions were statodont, composed of multicuspidate teeth added in distally diverging rows and through proximal superpositional replacement, while their symphyseal tooth whorls are comparable to chondrichthyan and osteichthyan counterparts. Ancestral state estimation indicates the presence of oral tubercles on the jaws of the gnathostome crown-ancestor; tooth whorls and/or tooth rows evolved independently in placoderms, osteichthyans, ischnacanthids, other acanthodians and crown-chondrichthyans. Crown-chondrichthyan dentitions are derived relative to the gnathostome crown-ancestor which possessed a simple dentition and lacked a permanent dental lamina which evolved independently in Chondrichthyes and Osteichthyes.

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U2 - 10.1038/s41559-021-01458-4

DO - 10.1038/s41559-021-01458-4

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VL - 5

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EP - 926

JO - Nature Ecology and Evolution

JF - Nature Ecology and Evolution

IS - 7

ER -

Acanthodian dental development and the origin of gnathostome dentitions

Abstract

Bibliographical note

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Teeth and jaws: evolutionary emergence of a model organogenic system and the adaptive radiation of gnathosomes.

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Data from Rücklin et al. 2021. Acanthodian dental development and the origin of gnathostome dentitions. Nature Ecology & Evolution

Cite this