Evolutionary Tinkering of the Mandibular Canal Linked to Convergent Regression of Teeth in Placental Mammals

International audience Loss or reduction of teeth has occurred independently in all major clades of mammals [1]. This process is associated with specialized diets, such as myrmecophagy and filter feeding [2, 3], and led to an extensive rearrangement of the mandibular anatomy. The mandibular canal en...

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Published in:Current Biology
Main Authors: Ferreira-Cardoso, Sérgio, Delsuc, Frédéric, Hautier, Lionel
Other Authors: Institut des Sciences de l'Evolution de Montpellier (UMR ISEM), Centre de Coopération Internationale en Recherche Agronomique pour le Développement (Cirad)-École Pratique des Hautes Études (EPHE), Université Paris Sciences et Lettres (PSL)-Université Paris Sciences et Lettres (PSL)-Université de Montpellier (UM)-Institut de recherche pour le développement IRD : UR226-Centre National de la Recherche Scientifique (CNRS), The Natural History Museum London (NHM), ANR-10-LABX-0004,CeMEB,Mediterranean Center for Environment and Biodiversity(2010), ANR-10-LABX-0020,NUMEV,Digital and Hardware Solutions and Modeling for the Environement and Life Sciences(2010)
Format: Article in Journal/Newspaper
Language:English
Published: HAL CCSD 2019
Subjects:
Online Access:https://hal.science/hal-02140102
https://hal.science/hal-02140102/document
https://hal.science/hal-02140102/file/Ferreira-Cardoso-CurrBiol-2019-HAL.pdf
https://doi.org/10.1016/j.cub.2018.12.023
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spelling ftecolephe:oai:HAL:hal-02140102v1 2024-05-19T07:38:02+00:00 Evolutionary Tinkering of the Mandibular Canal Linked to Convergent Regression of Teeth in Placental Mammals Ferreira-Cardoso, Sérgio Delsuc, Frédéric Hautier, Lionel Institut des Sciences de l'Evolution de Montpellier (UMR ISEM) Centre de Coopération Internationale en Recherche Agronomique pour le Développement (Cirad)-École Pratique des Hautes Études (EPHE) Université Paris Sciences et Lettres (PSL)-Université Paris Sciences et Lettres (PSL)-Université de Montpellier (UM)-Institut de recherche pour le développement IRD : UR226-Centre National de la Recherche Scientifique (CNRS) The Natural History Museum London (NHM) ANR-10-LABX-0004,CeMEB,Mediterranean Center for Environment and Biodiversity(2010) ANR-10-LABX-0020,NUMEV,Digital and Hardware Solutions and Modeling for the Environement and Life Sciences(2010) 2019 https://hal.science/hal-02140102 https://hal.science/hal-02140102/document https://hal.science/hal-02140102/file/Ferreira-Cardoso-CurrBiol-2019-HAL.pdf https://doi.org/10.1016/j.cub.2018.12.023 en eng HAL CCSD Elsevier info:eu-repo/semantics/altIdentifier/doi/10.1016/j.cub.2018.12.023 hal-02140102 https://hal.science/hal-02140102 https://hal.science/hal-02140102/document https://hal.science/hal-02140102/file/Ferreira-Cardoso-CurrBiol-2019-HAL.pdf doi:10.1016/j.cub.2018.12.023 info:eu-repo/semantics/OpenAccess ISSN: 0960-9822 EISSN: 1879-0445 Current Biology - CB https://hal.science/hal-02140102 Current Biology - CB, 2019, 29 (3), pp.468-475.e3. ⟨10.1016/j.cub.2018.12.023⟩ mandibular canal edentulous convergence mammals homology tooth development [SDV.BA.ZV]Life Sciences [q-bio]/Animal biology/Vertebrate Zoology [SDV.BID.EVO]Life Sciences [q-bio]/Biodiversity/Populations and Evolution [q-bio.PE] [SDV.BDD.MOR]Life Sciences [q-bio]/Development Biology/Morphogenesis info:eu-repo/semantics/article Journal articles 2019 ftecolephe https://doi.org/10.1016/j.cub.2018.12.023 2024-05-02T00:21:20Z International audience Loss or reduction of teeth has occurred independently in all major clades of mammals [1]. This process is associated with specialized diets, such as myrmecophagy and filter feeding [2, 3], and led to an extensive rearrangement of the mandibular anatomy. The mandibular canal enables lower jaw innervation through the passage of the inferior alveolar nerve (IAN) [4, 5]. In order to innervate teeth, the IAN projects ascending branches directly through tooth roots [5, 6], bone trabeculae [6], or bone canaliculi (i.e., dorsal canaliculi) [7]. Here, we used micro-computed tomography (μ-CT) scans of mandibles, from eight myrmecophagous species with reduced dentition and 21 non-myrmecophages, to investigate the evolutionary fate of dental innervation structures following convergent tooth regression in mammals. Our observations provide strong evidence for a link between the presence of tooth loci and the development of dorsal canaliculi. Interestingly, toothless anteaters present dorsal canaliculi and preserve intact tooth innervation, while equally toothless pangolins do not. We show that the internal mandibular morphology of anteaters has a closer resemblance to that of baleen whales [7] than to pangolins. This is despite masticatory apparatus resemblances that have made anteaters and pangolins a textbook example of convergent evolution. Our results suggest that early tooth loci innervation [8] is required for maintaining the dorsal innervation of the mandible and underlines the dorsal canaliculi sensorial role in the context of mediolateral mandibular movements. This study presents a unique example of convergent redeployment of the tooth developmental pathway to a strictly sensorial function following tooth regression in anteaters and baleen whales. Article in Journal/Newspaper baleen whales EPHE (Ecole pratique des hautes études, Paris): HAL Current Biology 29 3 468 475.e3
institution Open Polar
collection EPHE (Ecole pratique des hautes études, Paris): HAL
op_collection_id ftecolephe
language English
topic mandibular canal
edentulous
convergence
mammals
homology
tooth development
[SDV.BA.ZV]Life Sciences [q-bio]/Animal biology/Vertebrate Zoology
[SDV.BID.EVO]Life Sciences [q-bio]/Biodiversity/Populations and Evolution [q-bio.PE]
[SDV.BDD.MOR]Life Sciences [q-bio]/Development Biology/Morphogenesis
spellingShingle mandibular canal
edentulous
convergence
mammals
homology
tooth development
[SDV.BA.ZV]Life Sciences [q-bio]/Animal biology/Vertebrate Zoology
[SDV.BID.EVO]Life Sciences [q-bio]/Biodiversity/Populations and Evolution [q-bio.PE]
[SDV.BDD.MOR]Life Sciences [q-bio]/Development Biology/Morphogenesis
Ferreira-Cardoso, Sérgio
Delsuc, Frédéric
Hautier, Lionel
Evolutionary Tinkering of the Mandibular Canal Linked to Convergent Regression of Teeth in Placental Mammals
topic_facet mandibular canal
edentulous
convergence
mammals
homology
tooth development
[SDV.BA.ZV]Life Sciences [q-bio]/Animal biology/Vertebrate Zoology
[SDV.BID.EVO]Life Sciences [q-bio]/Biodiversity/Populations and Evolution [q-bio.PE]
[SDV.BDD.MOR]Life Sciences [q-bio]/Development Biology/Morphogenesis
description International audience Loss or reduction of teeth has occurred independently in all major clades of mammals [1]. This process is associated with specialized diets, such as myrmecophagy and filter feeding [2, 3], and led to an extensive rearrangement of the mandibular anatomy. The mandibular canal enables lower jaw innervation through the passage of the inferior alveolar nerve (IAN) [4, 5]. In order to innervate teeth, the IAN projects ascending branches directly through tooth roots [5, 6], bone trabeculae [6], or bone canaliculi (i.e., dorsal canaliculi) [7]. Here, we used micro-computed tomography (μ-CT) scans of mandibles, from eight myrmecophagous species with reduced dentition and 21 non-myrmecophages, to investigate the evolutionary fate of dental innervation structures following convergent tooth regression in mammals. Our observations provide strong evidence for a link between the presence of tooth loci and the development of dorsal canaliculi. Interestingly, toothless anteaters present dorsal canaliculi and preserve intact tooth innervation, while equally toothless pangolins do not. We show that the internal mandibular morphology of anteaters has a closer resemblance to that of baleen whales [7] than to pangolins. This is despite masticatory apparatus resemblances that have made anteaters and pangolins a textbook example of convergent evolution. Our results suggest that early tooth loci innervation [8] is required for maintaining the dorsal innervation of the mandible and underlines the dorsal canaliculi sensorial role in the context of mediolateral mandibular movements. This study presents a unique example of convergent redeployment of the tooth developmental pathway to a strictly sensorial function following tooth regression in anteaters and baleen whales.
author2 Institut des Sciences de l'Evolution de Montpellier (UMR ISEM)
Centre de Coopération Internationale en Recherche Agronomique pour le Développement (Cirad)-École Pratique des Hautes Études (EPHE)
Université Paris Sciences et Lettres (PSL)-Université Paris Sciences et Lettres (PSL)-Université de Montpellier (UM)-Institut de recherche pour le développement IRD : UR226-Centre National de la Recherche Scientifique (CNRS)
The Natural History Museum London (NHM)
ANR-10-LABX-0004,CeMEB,Mediterranean Center for Environment and Biodiversity(2010)
ANR-10-LABX-0020,NUMEV,Digital and Hardware Solutions and Modeling for the Environement and Life Sciences(2010)
format Article in Journal/Newspaper
author Ferreira-Cardoso, Sérgio
Delsuc, Frédéric
Hautier, Lionel
author_facet Ferreira-Cardoso, Sérgio
Delsuc, Frédéric
Hautier, Lionel
author_sort Ferreira-Cardoso, Sérgio
title Evolutionary Tinkering of the Mandibular Canal Linked to Convergent Regression of Teeth in Placental Mammals
title_short Evolutionary Tinkering of the Mandibular Canal Linked to Convergent Regression of Teeth in Placental Mammals
title_full Evolutionary Tinkering of the Mandibular Canal Linked to Convergent Regression of Teeth in Placental Mammals
title_fullStr Evolutionary Tinkering of the Mandibular Canal Linked to Convergent Regression of Teeth in Placental Mammals
title_full_unstemmed Evolutionary Tinkering of the Mandibular Canal Linked to Convergent Regression of Teeth in Placental Mammals
title_sort evolutionary tinkering of the mandibular canal linked to convergent regression of teeth in placental mammals
publisher HAL CCSD
publishDate 2019
url https://hal.science/hal-02140102
https://hal.science/hal-02140102/document
https://hal.science/hal-02140102/file/Ferreira-Cardoso-CurrBiol-2019-HAL.pdf
https://doi.org/10.1016/j.cub.2018.12.023
genre baleen whales
genre_facet baleen whales
op_source ISSN: 0960-9822
EISSN: 1879-0445
Current Biology - CB
https://hal.science/hal-02140102
Current Biology - CB, 2019, 29 (3), pp.468-475.e3. ⟨10.1016/j.cub.2018.12.023⟩
op_relation info:eu-repo/semantics/altIdentifier/doi/10.1016/j.cub.2018.12.023
hal-02140102
https://hal.science/hal-02140102
https://hal.science/hal-02140102/document
https://hal.science/hal-02140102/file/Ferreira-Cardoso-CurrBiol-2019-HAL.pdf
doi:10.1016/j.cub.2018.12.023
op_rights info:eu-repo/semantics/OpenAccess
op_doi https://doi.org/10.1016/j.cub.2018.12.023
container_title Current Biology
container_volume 29
container_issue 3
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