4.7 Article

Marsupials and Multi-Omics: Establishing New Comparative Models of Neural Crest Patterning and Craniofacial Development

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FRONTIERS MEDIA SA
DOI: 10.3389/fcell.2022.941168

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NCC; mammal; heterochrony; constraint; evolution; GRN; skull

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Studies on vertebrates have provided important insights into craniofacial morphogenesis, but little is known about the patterning of distinct facial morphologies during development. Comparative models between related species, such as mammals, can help uncover the origin of species-specific patterning. The use of single-cell multi-omics techniques allows for detailed investigation into the cellular and molecular processes underlying craniofacial evolution.
Studies across vertebrates have revealed significant insights into the processes that drive craniofacial morphogenesis, yet we still know little about how distinct facial morphologies are patterned during development. Studies largely point to evolution in GRNs of cranial progenitor cell types such as neural crest cells, as the major driver underlying adaptive cranial shapes. However, this hypothesis requires further validation, particularly within suitable models amenable to manipulation. By utilizing comparative models between related species, we can begin to disentangle complex developmental systems and identify the origin of species-specific patterning. Mammals present excellent evolutionary examples to scrutinize how these differences arise, as sister clades of eutherians and marsupials possess suitable divergence times, conserved cranial anatomies, modular evolutionary patterns, and distinct developmental heterochrony in their NCC behaviours and craniofacial patterning. In this review, I lend perspectives into the current state of mammalian craniofacial biology and discuss the importance of establishing a new marsupial model, the fat-tailed dunnart, for comparative research. Through detailed comparisons with the mouse, we can begin to decipher mammalian conserved, and species-specific processes and their contribution to craniofacial patterning and shape disparity. Recent advances in single-cell multi-omics allow high-resolution investigations into the cellular and molecular basis of key developmental processes. As such, I discuss how comparative evolutionary application of these tools can provide detailed insights into complex cellular behaviours and expression dynamics underlying adaptive craniofacial evolution. Though in its infancy, the field of comparative evo-devo-omics presents unparalleled opportunities to precisely uncover how phenotypic differences arise during development.

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