Integrative Analysis of Cellular Drivers of Color Diversification in Development and Evolution

During development, tissues are formed by the assembly of different cell types. Evolutionary changes in tissue phenotypes can be the result of mutations that alter the cell type composition or the cell types and their inherent properties. Although these are clear mechanistic links between development and evolution, most research has focused on the endpoints of the genotype-phenotype map, treating the cellular mechanisms that bridge genotype and phenotype as a black box. How changes in cell types contribute to the evolutionary change of tissues has been largely neglected, although it may be a key element driving phenotypic diversity. To study the role of cellular diversification in evolution, I will use a vertebrate system that has proven ideal for genotype-phenotype mapping: the species-rich and phenotypically diverse family of cichlid fishes. By focusing on a phenotypic trait (coloration) whose properties are directly linked to the cellular properties of a manageable number of pigment cell types, I will investigate the functional and mechanistic links that connect cellular changes to phenotypic changes arising during development (formation of distinct epithelial coloration traits) and evolution (formation of phenotypically diverse species). Using novel methodological approaches, I will phenotype cells in an integrative manner using a combination of single-cell RNA sequencing and high-throughput cellular phenotyping. The sufficiently (but not excessively) complex system of integumentary pigment cells is ideal for making concrete functional predictions about how cellular changes ultimately drive evolutionary change. This proposal will refine the concept of cell types and cellular variation in an evolutionary developmental context. It will pave the way for novel insights into how transcriptional changes drive the divergent and convergent evolution of cellular traits and thereby cause the emergence of tissue phenotypes.