title: Non-genetic diversity modulates population performance.
abstract: 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.
authors.affiliation: Department of Molecular, Cellular, and Developmental Biology, Yale University, New Haven, CT, USA.
authors.forename: Adam James
authors.identifier: http://orcid.org/0000-0002-3537-7313
authors.initials: AJ
authors.lastname: Waite
authors.affiliation: Department of Molecular, Cellular, and Developmental Biology, Yale University, New Haven, CT, USA.
authors.forename: Nicholas W
authors.initials: NW
authors.lastname: Frankel
authors.affiliation: Department of Molecular, Cellular, and Developmental Biology, Yale University, New Haven, CT, USA.
authors.forename: Yann S
authors.identifier: http://orcid.org/0000-0003-0244-0192
authors.initials: YS
authors.lastname: Dufour
authors.affiliation: Department of Molecular, Cellular, and Developmental Biology, Yale University, New Haven, CT, USA.
authors.forename: Jessica F
authors.identifier: http://orcid.org/0000-0001-6696-7909
authors.initials: JF
authors.lastname: Johnston
authors.affiliation: Department of Physics, Yale University, New Haven, CT, USA.
authors.forename: Junjiajia
authors.initials: J
authors.lastname: Long
authors.affiliation: Department of Molecular, Cellular, and Developmental Biology, Yale University, New Haven, CT, USA thierry.emonet@yale.edu.|Department of Physics, Yale University, New Haven, CT, USA.
authors.forename: Thierry
authors.identifier: http://orcid.org/0000-0002-6746-6564
authors.initials: T
authors.lastname: Emonet
mesh_terms: D000222:Adaptation, Physiological; D002633:Chemotaxis; D004926:Escherichia coli / Q000235:genetics / Q000502:physiology*; D029968:Escherichia coli Proteins / Q000378:metabolism*; D015964:Gene Expression Regulation, Bacterial; D046210:Microfluidic Analytical Techniques / Q000295:instrumentation*; D008954:Models, Biological; D010641:Phenotype
chemical_list: D029968:Escherichia coli Proteins
keywords: Jensen's inequality; cellular motility; chemotaxis; nonlinear systems; non‐genetic diversity