  Biological functions are typically performed by groups of cells that express
predominantly the same genes, yet display a continuum of phenotypes. While it
is known how one genotype can generate such non-genetic diversity, it remains
unclear how different phenotypes contribute to the performance of biological
function at the population level. We developed a microfluidic device to
simultaneously measure the phenotype and chemotactic performance of tens of
thousands of individual, freely-swimming Escherichia coli as they climbed a
gradient of attractant. We discovered that spatial structure spontaneously
emerged from initially well-mixed wild type populations due to non-genetic
diversity. By manipulating the expression of key chemotaxis proteins, we
established a causal relationship between protein expression, non- genetic
diversity, and performance that was theoretically predicted. This approach
generated a complete phenotype-to-performance map, in which we found a
nonlinear regime. We used this map to demonstrate how changing the shape of a
phenotypic distribution can have as large of an effect on collective
performance as changing the mean phenotype, suggesting that selection could act
on both during the process of adaptation.
