A model of replicating coupled oscillators generates naturally occurring cell networks

Abstract

ABSTRACT When a founder cell and its progeny divide with incomplete cytokinesis, a network forms in which each intercellular bridge corresponds to a past mitotic event. Such networks are required for gamete production in many animals, and different species have evolved diverse final network topologies. Although mechanisms regulating network assembly have been identified in particular organisms, we lack a quantitative framework to understand network assembly and inter-species variability. Motivated by cell networks responsible for oocyte production in invertebrates, where the final topology is typically invariant within each species, we devised a mathematical model for generating cell networks, in which each node is an oscillator and, after a full cycle, the node produces a daughter to which it remains connected. These cell cycle oscillations are transient and coupled via diffusion over the edges of the network. By variation of three biologically motivated parameters, our model generates nearly all such networks currently reported across invertebrates. Furthermore, small parameter variations can rationalize cases of intra-species variation. Because cell networks outside of the ovary often form less deterministically, we propose model generalizations to account for sources of stochasticity.