Quantifying the fitness contribution of phagocytosis

Phagocytosis, the ingestion of cells by other cells, is ubiquitous among eukaryotic life. It is required for food uptake in many single-celled species and for the immune response in multicellular species. The origin of phagocytosis and its role in the evolution of endomembranes and the eukaryotic cell remains obscure. Drawing on a wealth of empirical data, we integrate prey capture, engulfment, and internal and external digestion into a mathematical evolutionary model that quantifies the fitness of a primitive phagocytoser relative to a non-phagocytosing ancestor. We reveal the conditions under which a non-phagocytosing predator that digests its prey externally can persist. We also show that the phagocytoser can outperform the ancestor in a broad range of situations, despite the cost associated with producing a phagocytic cup. Parameter variations delineate how fast engulfment needs to be for phagocytosis to be advantageous, providing clear benchmarks for interpreting the importance of results in genetic knockout studies and mechanical models. The phagocytoser still outperforms the ancestor when food vacuoles can't fuse back to the plasma membrane, providing arguments in favor of the gradual evolution of phagocytosis and for phagocytosis as the initiator of the endomembrane system.