Abstract Populations of chemotactic bacteria can rapidly expand into new territory by consuming and chasing an attractant cue in the environment, increasing the population’s overall growth in nutrient-rich environments. Although the migrating fronts driving this expansion contain cells of multiple swimming phenotypes, the consequences of non-genetic diversity for population expansion are unknown. Here, through theory and simulations, we predict that expanding populations non-genetically adapt their phenotype composition to migrate effectively through multiple physical environments. Swimming phenotypes in the migrating front are spatially sorted by chemotactic performance, but the mapping from phenotype to performance depends on the environment. Therefore, phenotypes that perform poorly localize to the back of the group, causing them to selectively fall behind. Over cell divisions, the group composition dynamically enriches for high-performers, enhancing migration speed and overall growth. Furthermore, non-genetic inheritance controls a trade-off between large composition shifts and slow responsiveness to new environments, enabling a diverse population to out-perform a non-diverse one in varying environments. These results demonstrate that phenotypic diversity and collective behavior can synergize to produce emergent functionalities. Non-genetic inheritance may generically enable bacterial populations to transiently adapt to new situations without mutations, emphasizing that genotype-to-phenotype mappings are dynamic and context-dependent.

A mechanism for migrating bacterial populations to non-genetically adapt to new environments