Non-genetic adaptation of phenotypic diversity in migrating cell populations

In this talk I will report a novel mechanism that enables a migrating cell population to adapt its phenotypic composition to the environments it encounters without the need for regulation of gene expression or mutations.

Motile populations of isogenic cells must expand into diverse physical and chemical environments where different phenotypic traits are advantageous. To understand how motile populations adapt their phenotypic distribution to new environments, we studied the collective migration of chemotactic Escherichia coli. By measuring continuous distributions of swimming behaviors and chemoreceptor abundances prior to and during collective migration through diverse environments, we discovered that migrating cell populations rapidly tune their own phenotypic distributions in response to physical and chemical demands. This adaptation arises spontaneously from a dynamical balance between collective migration, which filters out cells with low chemotactic performance, and growth, which generates new phenotypes through cell division. Remarkably, we show that this adaptation mechanism acts simultaneously on multiple chemotaxis-associated traits.

This result introduces a new paradigm for population-level adaptation in biology. Mechanisms such as stochastic switching and regulating gene expression are fast (~1 generation) but are limited to the adaptation of a few phenotypic traits and often require dedicated pathways to implement. Adaptation by genetic mutations avoids these limitations but is slow (~10 generations). In contrast, standing variation in numerous phenotypic traits among individual cells is ubiquitous. Our finding demonstrates that adaptation by collective migration enables cell populations to adapt multiple traits rapidly and reversibly as they encounter new environments, thus offering a combination of speed and flexibility that is difficult to achieve via classical adaptation mechanisms.