Comparative transcriptomics in serial organs uncovers early and pan-organ developmental changes associated with organ-specific morphological adaptation

Abstract Mice have evolved a new dental plan with two additional cusps on the upper molar, while hamsters were retaining the ancestral plan. By comparing the dynamics of molar development with transcriptome time series, we found at least three early changes in mouse upper molar development. Together...

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Main Authors: Marie Sémon, Marion Mouginot, Manon Peltier, Claudine Corneloup, Philippe Veber, Laurent Guéguen, Sophie Pantalacci
Format: Article
Language:English
Published: Nature Portfolio 2025-01-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-025-55826-w
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author Marie Sémon
Marion Mouginot
Manon Peltier
Claudine Corneloup
Philippe Veber
Laurent Guéguen
Sophie Pantalacci
author_facet Marie Sémon
Marion Mouginot
Manon Peltier
Claudine Corneloup
Philippe Veber
Laurent Guéguen
Sophie Pantalacci
author_sort Marie Sémon
collection DOAJ
description Abstract Mice have evolved a new dental plan with two additional cusps on the upper molar, while hamsters were retaining the ancestral plan. By comparing the dynamics of molar development with transcriptome time series, we found at least three early changes in mouse upper molar development. Together, they redirect spatio-temporal dynamics to ultimately form two additional cusps. The mouse lower molar has undergone much more limited phenotypic evolution. Nevertheless, its developmental trajectory evolved as much as that of the upper molar and co-evolved with it. Among the coevolving changes, some are clearly involved in the new upper molar phenotype. We found a similar level of coevolution in bat limbs. In conclusion, our study reveals how serial organ morphology has adapted through organ-specific developmental changes, as expected, but also through shared changes that have organ-specific effects on the final phenotype. This highlights the important role of developmental system drift in one organ to accommodate adaptation in another.
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spelling doaj-art-136d5898127c4f73b094275b4aa12c922025-01-19T12:30:38ZengNature PortfolioNature Communications2041-17232025-01-0116111710.1038/s41467-025-55826-wComparative transcriptomics in serial organs uncovers early and pan-organ developmental changes associated with organ-specific morphological adaptationMarie Sémon0Marion Mouginot1Manon Peltier2Claudine Corneloup3Philippe Veber4Laurent Guéguen5Sophie Pantalacci6Laboratoire de Biologie et Modelisation de la Cellule, Ecole Normale Superieure de Lyon, CNRS, UMR 5239, Inserm, U1293, Universite Claude Bernard Lyon 1, 46 allee d’ItalieLaboratoire de Biologie et Modelisation de la Cellule, Ecole Normale Superieure de Lyon, CNRS, UMR 5239, Inserm, U1293, Universite Claude Bernard Lyon 1, 46 allee d’ItalieLaboratoire de Biologie et Modelisation de la Cellule, Ecole Normale Superieure de Lyon, CNRS, UMR 5239, Inserm, U1293, Universite Claude Bernard Lyon 1, 46 allee d’ItalieLaboratoire de Biologie et Modelisation de la Cellule, Ecole Normale Superieure de Lyon, CNRS, UMR 5239, Inserm, U1293, Universite Claude Bernard Lyon 1, 46 allee d’ItalieLaboratoire de Biometrie et Biologie Evolutive, Universite Claude Bernard Lyon 1, UMR CNRS 5558Laboratoire de Biometrie et Biologie Evolutive, Universite Claude Bernard Lyon 1, UMR CNRS 5558Laboratoire de Biologie et Modelisation de la Cellule, Ecole Normale Superieure de Lyon, CNRS, UMR 5239, Inserm, U1293, Universite Claude Bernard Lyon 1, 46 allee d’ItalieAbstract Mice have evolved a new dental plan with two additional cusps on the upper molar, while hamsters were retaining the ancestral plan. By comparing the dynamics of molar development with transcriptome time series, we found at least three early changes in mouse upper molar development. Together, they redirect spatio-temporal dynamics to ultimately form two additional cusps. The mouse lower molar has undergone much more limited phenotypic evolution. Nevertheless, its developmental trajectory evolved as much as that of the upper molar and co-evolved with it. Among the coevolving changes, some are clearly involved in the new upper molar phenotype. We found a similar level of coevolution in bat limbs. In conclusion, our study reveals how serial organ morphology has adapted through organ-specific developmental changes, as expected, but also through shared changes that have organ-specific effects on the final phenotype. This highlights the important role of developmental system drift in one organ to accommodate adaptation in another.https://doi.org/10.1038/s41467-025-55826-w
spellingShingle Marie Sémon
Marion Mouginot
Manon Peltier
Claudine Corneloup
Philippe Veber
Laurent Guéguen
Sophie Pantalacci
Comparative transcriptomics in serial organs uncovers early and pan-organ developmental changes associated with organ-specific morphological adaptation
Nature Communications
title Comparative transcriptomics in serial organs uncovers early and pan-organ developmental changes associated with organ-specific morphological adaptation
title_full Comparative transcriptomics in serial organs uncovers early and pan-organ developmental changes associated with organ-specific morphological adaptation
title_fullStr Comparative transcriptomics in serial organs uncovers early and pan-organ developmental changes associated with organ-specific morphological adaptation
title_full_unstemmed Comparative transcriptomics in serial organs uncovers early and pan-organ developmental changes associated with organ-specific morphological adaptation
title_short Comparative transcriptomics in serial organs uncovers early and pan-organ developmental changes associated with organ-specific morphological adaptation
title_sort comparative transcriptomics in serial organs uncovers early and pan organ developmental changes associated with organ specific morphological adaptation
url https://doi.org/10.1038/s41467-025-55826-w
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