Variation in Neural Crest Development and Functional Divergence of sox10 Paralogs Contribute to Morphological Diversification in Cichlid Fishes.

Neural crest (NC) is a vertebrate-specific embryonic progenitor cell population at the basis of important vertebrate features such as the craniofacial skeleton and pigmentation patterns. Despite the wide-ranging variation of NC-derived traits across vertebrates, the contribution of NC to species diversification remains largely unexplored. Here, by leveraging the adaptive diversity of African Great Lakes' cichlid species, we combined comparative transcriptomics and population genomics to investigate the role of NC development in morphological diversification. Our analysis revealed substantial differences in transcriptional landscapes across somitogenesis, an embryonic period coinciding with NC development and migration. Notably, several NC-related gene expression clusters showed both species-specific divergence in transcriptional landscapes and signatures of positive selection. Specifically, we identified two paralogs of the sox10 gene as prime NC-related candidates contributing to interspecific morphological variation, which displayed remarkable spatio-temporal expression variation in cichlids. Finally, through CRISPR-KO mutants, we experimentally validated the functional divergence between sox10 paralogs, with the acquisition of a novel role in cichlid skeletogenesis by sox10-like. Our study demonstrates the central role of NC-related processes - in particular those controlled by sox10s - in generating morphological diversification among closely-related species and lays the groundwork for further investigations into the mechanisms underpinning vertebrate NC diversification.