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Cheaters Lessen Colony Survival Under Stress in Yeast Experiment

Published: Thursday, May 02, 2013
Last Updated: Thursday, May 02, 2013
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MIT researchers find that high ratio of freeloaders makes it more likely colony will die from sudden shock to environment.

While a cooperative yeast colony that thrives by breaking down sucrose can survive with a high proportion of "cheaters" — or non-producers — such a mixed colony is less able to withstand sudden shock than a population made up purely of "cooperators," — or producers — researchers at MIT have shown.

In the first laboratory demonstration of an evolutionary-ecological feedback loop in a social, or cooperative, microbial population, physics postdoc Alvaro Sanchez and Assistant Professor of Physics Jeff Gore found that as the percentage of consumers grew relative to producers, they followed a spiral path toward equilibrium.

"One of the main things we were interested in was the idea that natural selection can have an effect on the ecology of a population, so that as a population is evolving, then natural selection affects the ecological properties of that population," Sanchez says.

They studied Saccharomyces cerevisiae, or baker's yeast, which is commonly used in making bread, beer and wine, and is a cooperative species that breaks down sucrose into glucose and fructose by expressing the enzyme invertase. The study focused on two variants of the yeast, a strain with the SUC2 gene that produces invertase, and a strain lacking SUC2, making it unable to produce the enzyme. About 88 percent of yeast that were sequenced in one study contained a gene coding for invertase, while about 12 percent were missing it.

Cheater cell advantage

Each single-celled yeast organism consumes only about 1 percent of the glucose it produces and enriches its environment by releasing the other 99 percent. That creates an opportunity for cheater cells, which lack the invertase gene, to consume the glucose. Because they aren't expending energy to break down sugar, cheater cells reproduce at a faster rate than cooperator cells, and soon outnumber them. The findings are published in the PLOS Biology article, "Feedback between population and evolutionary dynamics determines the fate of social microbial populations." To demonstrate the eco-evolutionary feedback loop in yeast, Sanchez ran a series of five different experiments.

"We were very surprised by the fact that the total population size for the mixed group is about the same at equilibrium as the total population size when there are no cheaters (purely cooperators). We didn't expect that," Sanchez says. Perhaps even more surprising, the mixed group could stabilize at a ratio of cheaters to cooperators of 9-to-1. "If we hadn't labeled the cheaters and cooperators differently, we wouldn't be able to tell that 90 percent of cells were taking advantage of the others," he says.

But when those stable populations were exposed by dilution to a suddenly harsh environment, in either one or two steps, all of the pure cooperator populations survived, while just one of six mixed populations adapted to fast deterioration, the report shows.

"The experiments of Sanchez and Gore beautifully illustrate the central dilemma in the evolution of cooperation. The yeast society depends on cooperation, but if cooperation is plentiful, 'cheaters' can exploit the generosity of others. This leads to cycles of cooperation and exploitation," says Benjamin Allen, assistant professor of mathematics at Emmanuel College.

Allen and Martin A. Nowak, director of the Program for Evolutionary Dynamics at Harvard University, co-authored an accompanying paper in PLOS Biology titled "Cooperation and the Fate of Microbial Societies."

Dynamic interplay

An eco-evolutionary feedback loop couples the effects of changes in population size with changes in the frequency of specific genetic types in the population. In the yeast populations under study, there was a dynamic interplay between evolution and ecology. As the population of cooperators grows, the environment changes as they consume sucrose and contribute more glucose to the environment, thus altering the ecological state. But the additional glucose allows cheaters to thrive and grow faster, thus altering the population dynamics as the proportion of cheaters to cooperators grows from the initial state. The increase in cheaters means there are proportionally fewer cooperators producing glucose to sustain the colony. Because the population consists of two different variants of the baker's yeast strain, one with a SUC2 gene (cooperators), and one without (cheaters), this genetic different can be represented as an evolutionary change as the population dynamic varies the proportion of one or the other variant in the population.

"They start in a sucrose environment where there is very little food that the cells can directly metabolize; they have to break it down first. So that gives some advantage to one of the two phenotypes, in this case, the cooperative phenotype. At first, the cooperative phenotype is very successful, but then as it transforms the environment; that harms itself from an evolutionary point of view. It gives an advantage now to the cheaters, so the cheaters now grow in the population. As they grow in the population, they also draw from the resources and that in turn further affects the evolutionary dynamics between cheaters and cooperators. The big idea here is that there is an interplay between the evolution of a gene and the environment where that evolution takes place. In this case, the population size and the availability of this public good. So there is this feedback loop between the two — evolution affects ecology and then ecology affects evolution," Sanchez says.

Fewer producers means less food, so cheaters lose their advantage and the overall population declines until the population of producers grows again allowing for the overall population to increase. That back and forth cycle is what creates the spiral effect observed in the experiment and marks the presence of a feedback loop.

"This idea of a feedback loop between evolution and ecology is a subject that's very exciting. It is more or less a recent idea, at least experimentally," Sanchez says. "In the case of cooperation, it is the first demonstration that this can actually happen."

Survival vs. extinction

The spiraling effect observed in the Sanchez-Gore experiments clearly demonstrated an eco-evolutionary feedback loop, Allen and Nowak says in the accompanying paper. "If there are sufficiently many cooperators in the initial population, the population converges in spiraling fashion to an equilibrium in which population density is high and cooperators and cheaters coexist." However, if the initial yeast population density or the initial proportion of cooperators (or both) is too low, not enough simple sugars are produced, and the colony dies. An area remaining to be explored is the effect of spatial structure on the evolution of cooperation in microbial colonies, Allen and Nowak says.

Sanchez conducted five separate experiments for five to eight days each on 60 independent cultures. "We repeated the experiment many times, and we get very reproducible results," Sanchez says.

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