title: Presence of a loner strain maintains cooperation and diversity in well-mixed bacterial communities.
abstract: Cooperation and diversity abound in nature despite cooperators risking exploitation from defectors and superior competitors displacing weaker ones. Understanding the persistence of cooperation and diversity is therefore a major problem for evolutionary ecology, especially in the context of well-mixed populations, where the potential for exploitation and displacement is greatest. Here, we demonstrate that a 'loner effect', described by economic game theorists, can maintain cooperation and diversity in real-world biological settings. We use mathematical models of public-good-producing bacteria to show that the presence of a loner strain, which produces an independent but relatively inefficient good, can lead to rock-paper-scissor dynamics, whereby cooperators outcompete loners, defectors outcompete cooperators and loners outcompete defectors. These model predictions are supported by our observations of evolutionary dynamics in well-mixed experimental communities of the bacterium Pseudomonas aeruginosa. We find that the coexistence of cooperators and defectors that produce and exploit, respectively, the iron-scavenging siderophore pyoverdine, is stabilized by the presence of loners with an independent iron-uptake mechanism. Our results establish the loner effect as a simple and general driver of cooperation and diversity in environments that would otherwise favour defection and the erosion of diversity.
authors.affiliation: Environmental Microbiology, Swiss Federal Institute of Aquatic Science and Technology (Eawag), Überlandstrasse 133, 8600 Dübendorf, Switzerland Department of Environmental Systems Science, ETH Zurich, Universitätsstrasse 16, 8092 Zürich, Switzerland.
authors.forename: R F
authors.initials: RF
authors.lastname: Inglis
authors.affiliation: Department of Plant Sciences, University of Oxford, South Parks Road, Oxford OX1 3RB, UK.
authors.forename: J M
authors.initials: JM
authors.lastname: Biernaskie
authors.affiliation: School of Biology, University of St Andrews, Dyers Brae, St Andrews KY16 9TH, UK.
authors.forename: A
authors.initials: A
authors.lastname: Gardner
authors.affiliation: Department of Plant and Microbial Biology, University of Zürich, Winterthurerstrasse 190, 8057 Zürich, Switzerland rolf.kuemmerli@uzh.ch.
authors.forename: R
authors.initials: R
authors.lastname: Kümmerli
mesh_terms: D044822:Biodiversity; D005075:Biological Evolution; D005716:Game Theory; D008962:Models, Theoretical; D009842:Oligopeptides / Q000096:biosynthesis / Q000378:metabolism*; D011157:Population Dynamics; D011549:Pseudomonas / Q000254:growth & development* / Q000378:metabolism; D011550:Pseudomonas aeruginosa / Q000254:growth & development / Q000378:metabolism
chemical_list: D009842:Oligopeptides; C042453:pyoverdin
keywords: experimental evolution; microbial biodiversity; non-transitive competition; rock–paper–scissor dynamics; siderophore; social evolution