A topological look into the evolution of developmental programs

Abstract

Rapid advance of experimental techniques provides an unprecedented in-depth view into complex developmental processes. Still, little is known on how the complexity of multicellular organisms evolved by elaborating developmental programs and inventing new cell types. A hurdle to understanding developmental evolution is the difficulty of even describing the intertwined network of spatiotemporal processes underlying the development of complex multicellular organisms. Nonetheless, an overview of developmental trajectories can be obtained from cell type lineage maps. Here, we propose that these lineage maps can also reveal how developmental programs evolve: the modes of evolving new cell types in an organism should be visible in its developmental trajectories, and therefore in the geometry of its cell type lineage map. This idea is demonstrated using a parsimonious generative model of developmental programs, which allows us to reliably survey the universe of all possible programs and examine their topological features. We find that, contrary to belief, tree-like lineage maps are rare and lineage maps of complex multicellular organisms are likely to be directed acyclic graphs where multiple developmental routes can converge on the same cell type. While cell type evolution prescribes what developmental programs come into existence, natural selection prunes those programs which produce low-functioning organisms. Our model indicates that additionally, lineage map topologies are correlated with such a functional property: the ability of organisms to regenerate. SIGNIFICANCE Cell type invention is a chief process in the evolution of developmental programs. Traditionally, developmental trajectories are represented as cell type lineage maps. Here we propose that systematic analysis of these maps, in particular their topology, should reveal traces of the manner in which cell types were invented. This is illustrated using a generative model of developmental programs, which allows one to robustly survey the geometry of cell lineage maps and link them to modes of cell type invention. We suggest that predictions made by such mathematical models, in conjunction with surveys of real cell-lineage maps of different multicellular lineages could uncover mechanisms underlying evolution of developmental programs.