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

• Published in: Nature communications 2025-01, Vol.16 (1), p.768-17, Article 768
• Main Authors: Sémon, Marie, Mouginot, Marion, Peltier, Manon, Corneloup, Claudine, Veber, Philippe, Guéguen, Laurent, Pantalacci, Sophie
• Format: Article
• Language: English
• Subjects: 13; 13/1; 13/51; 14; 14/63; 38; 38/39; 38/91; 45; 631/181/2481; 631/181/2806; 631/208/212/2019; 631/208/212/748; 64; Adaptation; Adaptation, Physiological - genetics; Animals; Biological Evolution; Chiroptera - anatomy & histology; Chiroptera - genetics; Chiroptera - growth & development; Coevolution; Cricetinae; Evolution & development; Female; Gene Expression Profiling; Gene Expression Regulation, Developmental; Hamsters; Humanities and Social Sciences; Male; Mice; Molar - anatomy & histology; Molar - growth & development; Molar - metabolism; Morphology; multidisciplinary; Organ Specificity; Phenotype; Phenotypes; Science; Science (multidisciplinary); Shape effects; Transcriptome; Transcriptomes; Transcriptomics
• ISSN: 2041-1723; 2041-1723
• DOI: 10.1038/s41467-025-55826-w

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. Mice evolved a new shape in the upper, but not in the lower molar. In addition to developmental changes specific to the upper molar, this occurred through shared changes with the lower molar, the development of which has drifted to support upper molar adaptation.