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Eco-evolutionary feedbacks can rescue cooperation in microbial populations

View Article: PubMed Central - PubMed

ABSTRACT

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 eco-evolutionary feedbacks can generate in microbial communities, feedbacks that reveal fundamental for the adaptive change of ecosystems at all scales.

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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 falling1221, 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).
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f1: 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 falling1221, 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).

Mentions: 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 interactions take place (Fig. S1). These interactions are modeled by means of a public good game with individual reproduction being set by the game payoff1221. Figure 1A displays a representative trajectory of the model: an increase of the cheating strain, due to its fitness advantage, causes a decrease in population density (less public good available). The demographic fall originates in the end variation in the composition of the groups, facilitating population assortment and the appearance of pure cooperator/cheater groups. Since the groups uniquely constituted by cooperators grow larger, they can ultimately reactivate the global population promoting again new cheater invasions. The whole process manifests in this way as a continuous cycle of decay and recovery of the community (Fig. 1A,B) (Materials and Methods). Demographic collapses consequently turn into an endogenous ecological mechanism that causes the required intergroup diversity, supporting the overall increase of cooperators −a mechanism that resembles a statistical phenomenon known as Simpson’s paradox1423.


Eco-evolutionary feedbacks can rescue cooperation in microbial populations
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 falling1221, 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).
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC5304172&req=5

f1: 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 falling1221, 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).
Mentions: 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 interactions take place (Fig. S1). These interactions are modeled by means of a public good game with individual reproduction being set by the game payoff1221. Figure 1A displays a representative trajectory of the model: an increase of the cheating strain, due to its fitness advantage, causes a decrease in population density (less public good available). The demographic fall originates in the end variation in the composition of the groups, facilitating population assortment and the appearance of pure cooperator/cheater groups. Since the groups uniquely constituted by cooperators grow larger, they can ultimately reactivate the global population promoting again new cheater invasions. The whole process manifests in this way as a continuous cycle of decay and recovery of the community (Fig. 1A,B) (Materials and Methods). Demographic collapses consequently turn into an endogenous ecological mechanism that causes the required intergroup diversity, supporting the overall increase of cooperators −a mechanism that resembles a statistical phenomenon known as Simpson’s paradox1423.

View Article: PubMed Central - PubMed

ABSTRACT

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 eco-evolutionary feedbacks can generate in microbial communities, feedbacks that reveal fundamental for the adaptive change of ecosystems at all scales.

No MeSH data available.


Related in: MedlinePlus