Collective migration is a key feature of the social amoebae Dictyostelium discoideum, where the binding of chemoattractants leads to the production and secretion of additional chemoattractant and the relay of the signal to neighboring cells. This then guides cells to migrate collectively in a head-to-tail fashion. We used mutants that were defective in signal relay to elucidate which quantitative metrics of cell migration are most strongly affected by signal relay and collective motion. We show that neither signal relay nor collective motion markedly impact the speed of cell migration. Cells maintained a preferred overall direction of motion for several minutes with similar persistence, regardless of whether or not they were attracted to moving neighbors, moving collectively in contact with their neighbors, or simply following a fixed exogenous signal. We quantitatively establish that signal relay not only increases the number of cells that respond to a chemotactic signal, but most remarkably, also transmits information about the location of the source accurately over large distances, independently of the strength of the exogenous signal. We envision that signal relay has a similar key role in the migration of a variety of chemotaxing mammalian cells that can relay chemoattractant signals.