feedback between population and evolutionary dynamics determines the fate of social microbial populations.

Feedback between Population and Evolutionary Dynamics Determines the Fate of Social Microbial Populations Alvaro Sanchez*, Jeff Gore* Department of Physics, Massachusetts Institute of Technology, Cambridge, Massachusetts, United States of America Abstract The evolutionary spread of cheater strategies can destabilize populations engaging in social cooperative behaviors, thus demonstrating that evolutionary changes can have profound implications for population dynamics. At the same time, the relative fitness of cooperative traits often depends upon population density, thus leading to the potential for bi-directional coupling between population density and the evolution of a cooperative trait. Despite the potential importance of these eco-evolutionary feedback loops in social species, they have not yet been demonstrated experimentally and their ecological implications are poorly understood. Here, we demonstrate the presence of a strong feedback loop between population dynamics and the evolutionary dynamics of a social microbial gene, SUC2, in laboratory yeast populations whose cooperative growth is mediated by the SUC2 gene. We directly visualize eco-evolutionary trajectories of hundreds of populations over 50–100 generations, allowing us to characterize the phase space describing the interplay of evolution and ecology in this system. Small populations collapse despite continual evolution towards increased cooperative allele frequencies; large populations with a sufficient number of cooperators ‘‘spiral’’ to a stable state of coexistence between cooperator and cheater strategies. The presence of cheaters does not significantly affect the equilibrium population density, but it does reduce the resilience of the population as well as its ability to adapt to a rapidly deteriorating environment. Our results demonstrate the potential ecological importance of coupling between evolutionary dynamics and the population dynamics of cooperatively growing organisms, particularly in microbes. Our study suggests that this interaction may need to be considered in order to explain intraspecific variability in cooperative behaviors, and also that this feedback between evolution and ecology can critically affect the demographic fate of those species that rely on cooperation for their survival. Citation: Sanchez A, Gore J (2013) Feedback between Population and Evolutionary Dynamics Determines the Fate of Social Microbial Populations. PLoS Biol 11(4): e1001547. doi:10.1371/journal.pbio.1001547 Academic Editor: Stephen P. Ellner, Cornell University, United States of America Received November 9, 2012; Accepted March 14, 2013; Published April 30, 2013 Copyright: ß 2013 Sanchez, Gore. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Funding: This work was supported by grant FQEB #RFP-12-07, NIH grants NIH DP2 and R00 GM085279-02, and grant PHY-1055154 from the NSF. The authors also received support from the Pew Foundation and the Alfred P. Sloan Foundation. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing Interests: The authors have declared that no competing interests exist. * E-mail: (AS); (JG) Cooperative species can be challenged by the emergence of intraspecific ‘‘cheaters’’ which take advantage of the common good produced by the community but do not contribute to its production. As a result, the cheaters may have higher fitness than cooperators and proliferate in the population at the expense of cooperators. The decline in cooperator numbers driven by evolutionary competition with the cheaters can have strong ecological consequences, as the ability of the population to produce the common good may be compromised [13]. These interactions have been predicted theoretically to yield an ecoevolutionary feedback between the allele frequency of a cooperative gene and the population size [7,8,10,14]. However, this bidirectional feedback has not been demonstrated experimentally, and the ecological consequences of such feedback are not known. Microbes are remarkably social organisms [15], and are also amenable to laboratory experimentation [16–18]. Very often, microbial cooperation results from the secretion of extracellular molecules or ‘‘public goods’’ to the media, such as quorum sensing molecules, extracellular enzymes, or the polymers that make up the fabric of biofilms. In some microbial species, population dynamics has been found to influence the evolution of cooperation Introduction Evolutionary changes in a species can strongly affect its environment over the timescales where speciation typically occurs. While this long-term effect of evolution on ecology has been long appreciated, it is typically assumed that evolutionary changes occur over timescales that are too long to affect the dynamics of population size in the short term [1]. For this reason, most models of population biology ignore evolutionary changes in the different species (e.g., predator/prey models), implicitly assuming a separation of timescales between population dynamics and evolutionary dynamics [2]. However, recent studies in several wild populations suggest that changes in allele frequency can occur over timescales that are comparable to those typical of population dynamics [1,3–6]. Given this overlap in timescales, evolutionary dynamics and population dynamics may be coupled in what has been termed an eco-evolutionary feedback loop [1,3]. These eco-evolutionary feedback loops are predicted to be particularly strong in cooperatively growing species [7–11], which produce common goods and typically have larger fitness at large population densities than at low population densities [12–14]. PLOS Biology | www.plosbiology.org 1 April 2013 | Volume 11 | Issue 4 | e1001547 Eco-evolutionary Feedback in Social Microbial Gene (Figure 1A and 1B; Materials and Methods) [14,22]. In the absence of evolutionary dynamics (SUC2 gene frequency of 100%), we observe either rapid collapse or rapid approach to a stable population size, depending on the starting population size. The effect of SUC2 evolutionary dynamics on the population dynamics was assessed by growing mixed cultures of SUC2 carriers (cooperators) and a second strain with a SUC2 deletion (cheaters) [22]. Each strain was transformed with a fluorescent protein of different color, so cheaters and cooperators could be discriminated by flow cytometry (see Materials and Methods). Four cultures were inoculated with different initial SUC2 frequencies (from f = 0.05 to f = 0.5) and initial cell densities ranging from N = 103 to N = 104 cells/ml, and were then subject to a daily growth-dilution cycle (6676 dilution factor) for 5 days. We found that the population dynamics are much more complicated than they (...truncated)