Leader cells in collective chemotaxis: optimality and trade-offs*

Clusters of cells can work together in order to follow a signal gradient, chemotaxing even when single cells do not. This behavior is robust over many cell types and many signals. Cells in different regions of migrating streams show different gene expression, suggesting cells specialize to leader and follower roles in collective chemotaxis. We use a simple mathematical model to find when specialization would be advantageous. In our model, leader cells sense the gradient with an accuracy that depends on the kinetics of ligand-receptor binding while follower cells attempt to follow the cluster's direction with a finite error. Intuitively, specialization into leaders and followers should be optimal when a few cells have much more information than the rest of the cluster, such as in the presence of a sharp transition from one chemical concentration to another. We do find this - but also find that high levels of specialization can be optimal in the opposite limit of a very shallow gradient. There is also an important tradeoff: clusters have to choose between speed in following a gradient and ability to reorient quickly.