Non-genetic adaptation by collective migration

Cell populations must adjust their phenotypic composition to adapt to
changing environments. One adaptation strategy is to maintain distinct
phenotypic subsets within the population and to modulate their relative
abundances via gene regulation. Another strategy involves genetic
mutations, which can be augmented by stress-response pathways. Here, we
studied how a migrating bacterial population regulates its phenotypic
distribution to traverse diverse environments. We generated isogenic
Escherichia coli populations with varying distributions of swimming
behaviors and observed their phenotype distributions during migration in
liquid and porous environments. We found that the migrating populations
became enriched with high-performing swimming phenotypes in each
environment, allowing the populations to adapt without requiring mutations
or gene regulation. This adaptation is dynamic and rapid, reversing in a
few doubling times when migration ceases. By measuring the chemoreceptor
abundance distributions during migration towards different attractants, we
demonstrated that adaptation acts on multiple chemotaxis-related traits
simultaneously. These measurements are consistent with a general mechanism
in which adaptation results from a balance between cell growth generating
diversity and collective migration eliminating under-performing
phenotypes. Thus, collective migration enables cell populations with
continuous, multi-dimensional phenotypes to flexibly and rapidly adapt
their phenotypic composition to diverse environmental conditions.