Competition between species can stabilize public-goods cooperation within a species

Abstract

Competition between species is a major ecological force that can drive evolution. Here, we test the effect of this force on the evolution of cooperation within a species. We use sucrose metabolism of budding yeast, Saccharomyces cerevisiae, as a model cooperative system that is subject to social parasitism by cheater strategies. We find that when cocultured with a bacterial competitor, Escherichia coli, the frequency of cooperator phenotypes in yeast populations increases dramatically as compared with isolated yeast populations. Bacterial competition stabilizes cooperation within yeast by limiting the yeast population density and also by depleting the public goods produced by cooperating yeast cells. Both of these changes induced by bacterial competition increase the cooperator frequency because cooperator yeast cells have a small preferential access to the public goods they produce; this preferential access becomes more important when the public good is scarce. Our results indicate that a thorough understanding of species interactions is crucial for explaining the maintenance and evolution of cooperation in nature.

Figure 1

When cocultured with bacteria in sucrose media, cooperator cell fraction increases within yeast populations. Both with E. coli strains DH5α or JM1100—a mutant strain that grows poorly on glucose and fructose—a significant increase in cooperator fraction was observed compared with a pure yeast culture (isolated yeast) over 10 days of growth. Addition of excess glucose (+0.2%) to these cultures eliminated this increase in cooperator fraction, indicating that selection for cooperators is linked to sucrose metabolism. In this experiment, culture media contained 4 mM buffer (PIPES). Total final yeast and bacterial densities did not change significantly over the course of five cycles of growth (Supplementary Figure S9). Error bars, ±s.e.m. (n=3). Source data is available for this figure in the Supplementary Information.

Figure 2

Correlation between the intensity of interspecific competition and cooperator cell frequency within yeast. (A) Successional growth dynamics in mixed cultures of yeast and bacteria. Absorbance (600 nm) was measured for different buffer (PIPES) concentrations: 4 mM (circles), 8 mM (triangles), and 12 mM (diamonds). Simultaneously, fluorescence of a pH-sensitive dye (fluorescein) was measured and a sharp pH drop was observed coinciding with bacterial growth. Note that as the buffering increases, the pH drop is slower and the final bacterial biomass is higher. Initial pH was 6.5 (∼220 fluorescence a.u.) in all the cultures used in our experiments (see Materials and methods and Supplementary Figure S5B). (B) Frequency of cooperators within yeast increases faster with increasing buffer concentration when competing against bacteria. Isolated control populations under the same conditions displayed little change in cooperator fraction (orange symbols). (C) Yeast (triangles) and bacterial (circles) density at the end of the last growth cycle as a function of buffering capacity. (D) Yeast density versus bacterial density across all buffer concentrations and different initial cooperator fractions for each cycle (initial fractions: 0.1, 0.3, 0.5, and 0.9). Control cultures (isolated yeast) for the same conditions are shown in triangles. Error bars, ±s.e.m. (n=3). Source data is available for this figure in the Supplementary Information.

Figure 3

A phenomenological model describes the growth dynamics of cooperator and cheater yeast during each cycle of batch culture. This sketch of our yeast growth model describes how the per capita growth rate changes as a function of yeast density. At low density, cooperators have a higher growth rate than defectors. Above a yeast density N_C where cooperator density is at a critical value, it is assumed that the growth rate is higher for both cooperators and cheaters as glucose has accumulated in the media (Gore et al, 2009). Then, the growth rate decreases logistically to zero as the yeast density reaches its carrying capacity, K. If the yeast-carrying capacity was limited (K_new), starting yeast density would be lower after dilution into fresh media.

Figure 4

Nutrient limitation can select for cooperator cells within the yeast population even in the absence of bacteria. Limiting either uracil (A) or phosphate (B) increases frequency of cooperators within isolated yeast populations. Control cultures (gray symbols) with excess glucose (0.2%) displayed negligible change in cooperator frequency. (C) Final cooperator fraction versus final yeast density in bacterial competition and nutrient-limitation experiments: DH5α, JM1100, uracil, and phosphate. Note that for both of the limiting nutrients (uracil and phosphate), yeast density versus cooperator fraction relationships are extremely similar, indicating that the underlying force for increase in cooperator fraction is the limited carrying capacity. With controls: uracil+0.2% Glucose (gray triangles) and phosphate+0.2% Glucose (gray squares). Controls (isolated yeast) for competition with bacteria are shown in orange circles and diamonds for DH5α and JM1100 conditions, respectively. Solid lines are model simulations for each condition. Error bars, ±s.e.m. (n=3). Source data is available for this figure in the Supplementary Information