Investigating evolutionary and developmental cellular trajectories with single-cell phylotranscriptomics

Multicellular organisms achieve their complexity through a rich diversity of cell types, each performing specialized roles within the organism. As the fundamental units of form and function, cell types offer a compelling vantage point for investigating how developmental processes intersect with evolutionary history. The gene expression programs that define each cell type encode not only their functional identities but also carry molecular signatures of evolutionary constraint and innovation. For a long time, efforts to dissect these programs were limited by the resolution of traditional bulk transcriptomic approaches. The advent of single-cell transcriptomics now enables these programs to be examined at cellular resolution, allowing the study of cell type gene expression patterns across both developmental and evolutionary timescales. This breakthrough opens the possibility to address longstanding questions in evolutionary developmental biology (evo-devo), such as how novel cell types emerge and how ontogeny relates to phylogeny. Among multicellular lineages, vertebrates stand out for their remarkable morphological complexity and extensive cellular diversity, making them ideal for exploring these evo-devo questions. In this thesis, I design a single-cell phylotranscriptomic approach that combines single-cell transcriptomics with gene evolutionary origins to uncover molecular evolutionary signatures embedded within cell type-specific gene expression programs. By applying this strategy, I elucidate mechanisms of cell type evolution, including how the recruitment of taxonomically restricted genes (TRGs) contributes to novel cell type identity, and reveal the cellular basis of the molecular hourglass pattern in vertebrate development. Overall, this work advances our understanding of the interplay between evolution and development at the level of cellular gene expression.

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