Eco-evolutionary feedbacks can rescue cooperation in microbial populations

www.nature.com/scientificreports OPEN received: 24 November 2016 accepted: 12 January 2017 Published: 13 February 2017 Eco-evolutionary feedbacks can rescue cooperation in microbial populations Clara Moreno-Fenoll1, Matteo Cavaliere1,2, Esteban Martínez-García3 & Juan F. Poyatos1 Bacterial populations whose growth depends on the cooperative production of public goods are usually threatened by the rise of cheaters that do not contribute but just consume the common resource. Minimizing cheater invasions appears then as a necessary mechanism to maintain these populations. However, that invasions result instead in the persistence of cooperation is a prospect that has yet remained largely unexplored. Here, we show that the demographic collapse induced by cheaters in the population can actually contribute to the rescue of cooperation, in a clear illustration of how ecology and evolution can influence each other. The effect is made possible by the interplay between spatial constraints and the essentiality of the shared resource. We validate this result by carefully combining theory and experiments, with the engineering of a synthetic bacterial community in which the public compound allows survival to a lethal stress. The characterization of the experimental system identifies additional factors that can matter, like the impact of the lag phase on the tolerance to stress, or the appearance of spontaneous mutants. Our work explains the unanticipated dynamics that ecoevolutionary feedbacks can generate in microbial communities, feedbacks that reveal fundamental for the adaptive change of ecosystems at all scales. In many bacterial populations, resources produced by an individual may benefit other members of the population. These resources generally entail compounds secreted into the environment, which in effect work as public goods. Classical examples comprise molecules that can specify the precise density reached by a population (quorum-sensing autoinducers)1, support the assemblage of collective multicellular structures (biofilms extracellular polymeric substances)2, or process basic nutrients that would be unavailable otherwise (iron-scavenging siderophores, exoenzymes catalyzing the decomposition of complex sugars, etc.)3,4. Notably, the functions of these, and equivalent, public goods are constantly at the risk of being disabled by the invasion of cheaters in the population, individuals that do not contribute and only reap the advantages of the common resource5–8. The threat of cheaters represents at a microbial scale a well-known public-good dilemma, known as the tragedy of the commons9, and can fundamentally interfere with the sustainability of these communities. With their particular relevance to humans in matters of health (microbiome)10, and industry (bioremediation, biofuels, etc)11, the necessity of recognizing the consequences of social dilemmas in microorganisms becomes even more significant. Much previous work focused therefore on identifying mechanisms that prevent the invasion of cheaters7. Here, we show how cheating can instead induce the continuance of cooperation, a prospect that has yet remained largely unexplored6. This is linked to the synergistic effects of spatial structure and eco-evolutionary feedbacks, that impact in a nonintuitive manner on the dilemma12,13. We considered specifically a scenario where a bacterial community is organized as a dynamical metapopulation (i.e., the community is transiently separated into groups, adding to other implementations of spatial structure such as groups connected via migration, and range expansions)14–16, and a public good is essential for its survival. Spatial structure is a well-known universal mechanism to promote cooperation17, which frequently emerges in bacterial populations, for instance, due to the restricted range of microbial interactions18,19. However, it is much less understood how the presence of structure affects the maintenance of cooperation when combined with explicit population dynamics (earlier work usually assumed constant population and only examined evolutionary dynamics)20. The change in population size associated to the essentiality of the public good can indeed bring about complex eco-evolutionary feedbacks12,13,21, in which both population density –ecological dynamics– and frequency of 1 Logic of Genomics Systems Lab (CNB-CSIC), Madrid, Spain. 2BBSRC/EPSRC/MRC Synthetic Biology Research Centre, University of Edinburgh, Edinburgh, UK. 3Molecular Environmental Microbiology Lab (CNB-CSIC) Madrid, Spain. Correspondence and requests for materials should be addressed to J.F.P. (email: ) Scientific Reports | 7:42561 | DOI: 10.1038/srep42561 1 www.nature.com/scientificreports/ Figure 1. Exploitation by cheaters contributes to the rescue of cooperation. (A) Typical population dynamics obtained with an in silico model of a microbial community, which is organized as a transient metapopulation (Fig. S1) (Materials and Methods). Growth depends on an essential public good produced by the “cooperator” individuals. When “cheaters” invade, the decline in the amount of public good drives the collapse of the total population. This collapse paradoxically determines its subsequent revival. (B) Revival is coupled to the endogenous emergence of variability in the composition of the groups (constituting the metapopulation) when the population is falling12,21, and the following occurrence of groups only constituted by cooperators. For the time window highlighted in (A), we display group composition (bottom; ratio of cooperators on each group is colored according to the gradient shown; white squares denote empty groups, of a total of N = 30), intergroup diversity (top; black curve, quantified as variance in group composition), and number of empty groups (top; pink curve). cooperators –evolutionary dynamics– influence each other. The connection between these feedbacks and spatial structure has been theoretically described to allow the dynamical persistence of cooperation15 but largely remains an open problem that has started to be experimentally addressed only recently22–25. We show in this work how such connection can direct to the unexpected consequence that the population collapse linked to cheater invasions eventually generates conditions that contribute to the revival of cooperators. This represents, more broadly, an example of the effects that both ecological and evolutionary forces can generate on community dynamics when acting on similar scales26,27. Results Eco-evolutionary dynamics. To analyze this scenario, we first introduced a stylized in silico model considering an initial finite population of agents –representing bacteria– with a given frequency of cooperators (producers of a public good, with a fitness cost) and cheaters (nonproducers, that could have emerged originally from the cooperators by mutation) (Materials and Methods). The population is temporarily organized in groups, where inte (...truncated)