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 in which multiple developmental routes can converge on the same cell type. Although cell type evolution prescribes what developmental programs come into existence, natural selection prunes those programs that 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.

Two-way exchanges between animal and plant biology, with focus on evo-devo

“…According to a traditional perspective, "to study development is to study multicellularity" (Bonner, 2001). However, the exclusion of unicells from developmental biology is unwarranted (Minelli, 2020;Mani and Tlusty, 2021;Minelli and Valero-Gracia, 2022). Along their life cycles, several unicells undergo dramatic and predictable transitions, besides those corresponding to progression along the mitotic cycle (e.g., Bozdech et al, 2003;Matthews, 2005;Ehrenkaufer et al, 2007;Kabani et al, 2009;Dayel et al, 2011;Fairclough et al, 2013;Sebé-Pedrós et al, 2016).…”

Spatially and Temporally Distributed Complexity—A Refreshed Framework for the Study of GRN Evolution

“…According to a traditional perspective, “to study development is to study multicellularity” [ 41 ]. However, the exclusion of unicells from developmental biology is unwarranted [ 42 ]. Along their life cycles, several unicells undergo dramatic and predictable transitions, besides those corresponding to progression along the mitotic cycle.…”

“…However, the application of this framework may skew the resulting tree-like topology. This bias has possibly historical roots [ 42 ] in the tree-like topology map used to describe the cell lineage of Caenorhabditis elegans , the first ever constructed [ 84 ]. Hence, algorithms used to infer lineage maps are biased toward the production of tree-like and chain-like topologies [ 85 ].…”

“…This would imply that cell-type lineage graphs are unlikely to be tree-like [ 86 ]. Instead, the most common would be acyclic graphs where multiple developmental routes end up at the same cell type [ 42 ]. Examples of nontree-like lineage maps have been reported for zebrafish development [ 87 ] and hydra adult homeostasis [ 88 ].…”

Cellular gradient flow structure connects single-cell-level rules and population-level dynamics

“…Moreover, the multiple cell types are hierarchically ordered, and their kinetic properties, e.g., type-switching and proliferation rates, also seem to be coupled. The existence of hierarchy, or equivalently, acyclic cell-type lineage structures and kinetic coupling are prevalent in multicellular systems from immunity to development [4][5][6][7]. These single-cell rules emerging in a population may be related to the functions and the coordination of the population.…”