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Is bacterial persistence a social trait?

Gardner A, West SA, Griffin AS - PLoS ONE (2007)

Bottom Line: Persistence has a direct benefit to cells because it allows survival during catastrophes-a form of bet-hedging.However, persistence can also provide an indirect benefit to other individuals, because the reduced growth rate can reduce competition for limiting resources.More generally, our results clarify the links between persistence and other bet-hedging or social behaviours.

View Article: PubMed Central - PubMed

Affiliation: St John's College, Oxford University, Oxford, United Kingdom. andy.gardner@ed.ac.uk

ABSTRACT
The ability of bacteria to evolve resistance to antibiotics has been much reported in recent years. It is less well-known that within populations of bacteria there are cells which are resistant due to a non-inherited phenotypic switch to a slow-growing state. Although such 'persister' cells are receiving increasing attention, the evolutionary forces involved have been relatively ignored. Persistence has a direct benefit to cells because it allows survival during catastrophes-a form of bet-hedging. However, persistence can also provide an indirect benefit to other individuals, because the reduced growth rate can reduce competition for limiting resources. This raises the possibility that persistence is a social trait, which can be influenced by kin selection. We develop a theoretical model to investigate the social consequences of persistence. We predict that selection for persistence is increased when: (a) cells are related (e.g. a single, clonal lineage); and (b) resources are scarce. Our model allows us to predict how the level of persistence should vary with time, across populations, in response to intervention strategies and the level of competition. More generally, our results clarify the links between persistence and other bet-hedging or social behaviours.

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The evolution of persister function, with less extreme differences in persister and nonpersister survival and growth, and differences in efficiency of resource use.(A) ESS persister allocation (π*) is a decreasing function of the relative survival (s) of nonpersister cells. We assume: p0 = 1, T = 5, g = 0, a = 1 and a range of z0. (B) ESS persister allocation (π*) is an increasing function of the relative growth rate (g) of persister cells. We assume: p0 = 1, T = 5, s = 0, a = 1 and a range of z0. (C) ESS persister allocation (π*) may depend on the relative competitive strain on resources imposed by persister cells (a), but this is negligible when they appear only infrequently in bacterial populations (low π*). We assume: p0 = 1, T = 5, s = 0, g = 0 and a range of z0.
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pone-0000752-g004: The evolution of persister function, with less extreme differences in persister and nonpersister survival and growth, and differences in efficiency of resource use.(A) ESS persister allocation (π*) is a decreasing function of the relative survival (s) of nonpersister cells. We assume: p0 = 1, T = 5, g = 0, a = 1 and a range of z0. (B) ESS persister allocation (π*) is an increasing function of the relative growth rate (g) of persister cells. We assume: p0 = 1, T = 5, s = 0, a = 1 and a range of z0. (C) ESS persister allocation (π*) may depend on the relative competitive strain on resources imposed by persister cells (a), but this is negligible when they appear only infrequently in bacterial populations (low π*). We assume: p0 = 1, T = 5, s = 0, g = 0 and a range of z0.

Mentions: From an evolutionary perspective, the key problem with persistence is the trade-off between survival and growth. Persistence is beneficial because it allows survival through catastrophic events, but is costly because it leads to lower growth rate. Our aim is to determine the evolutionarily stable strategy (ESS; [21]) for proportional allocation to persister function (π*) for given situations, i.e. as a function of model parameters (z0, p0 and T). This is the strategy that is the best response to itself; in other words, when all members of the metapopulation adopt the ESS, each individual maximizes its fitness by adopting the ESS, and those that employ a variant strategy do not achieve higher fitness. Consequently, when the metapopulation is not at an ESS, rare variants adopting different persister strategies can invade, and when the majority of individuals adopt the ESS, no other persister strategy can invade from rarity. In Appendix S1, we calculate how persister strategies relate to growth and survival through catastrophe events, and hence Darwinian fitness, and arrive at an implicit solution for the ESS:(1)This can be solved explicitly for numerical parameter values (Figure 2). The same procedure can be used to derive numerical solutions for the extended models incorporating random waiting times until catastrophe (Appendix S1, and Figure 3), less extreme differences between persister and nonpersister cells in their growth or survival rates, and differences in the competitive strain that they exert upon the population's resources (Appendix S1, and Figure 4).


Is bacterial persistence a social trait?

Gardner A, West SA, Griffin AS - PLoS ONE (2007)

The evolution of persister function, with less extreme differences in persister and nonpersister survival and growth, and differences in efficiency of resource use.(A) ESS persister allocation (π*) is a decreasing function of the relative survival (s) of nonpersister cells. We assume: p0 = 1, T = 5, g = 0, a = 1 and a range of z0. (B) ESS persister allocation (π*) is an increasing function of the relative growth rate (g) of persister cells. We assume: p0 = 1, T = 5, s = 0, a = 1 and a range of z0. (C) ESS persister allocation (π*) may depend on the relative competitive strain on resources imposed by persister cells (a), but this is negligible when they appear only infrequently in bacterial populations (low π*). We assume: p0 = 1, T = 5, s = 0, g = 0 and a range of z0.
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Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC1937027&req=5

pone-0000752-g004: The evolution of persister function, with less extreme differences in persister and nonpersister survival and growth, and differences in efficiency of resource use.(A) ESS persister allocation (π*) is a decreasing function of the relative survival (s) of nonpersister cells. We assume: p0 = 1, T = 5, g = 0, a = 1 and a range of z0. (B) ESS persister allocation (π*) is an increasing function of the relative growth rate (g) of persister cells. We assume: p0 = 1, T = 5, s = 0, a = 1 and a range of z0. (C) ESS persister allocation (π*) may depend on the relative competitive strain on resources imposed by persister cells (a), but this is negligible when they appear only infrequently in bacterial populations (low π*). We assume: p0 = 1, T = 5, s = 0, g = 0 and a range of z0.
Mentions: From an evolutionary perspective, the key problem with persistence is the trade-off between survival and growth. Persistence is beneficial because it allows survival through catastrophic events, but is costly because it leads to lower growth rate. Our aim is to determine the evolutionarily stable strategy (ESS; [21]) for proportional allocation to persister function (π*) for given situations, i.e. as a function of model parameters (z0, p0 and T). This is the strategy that is the best response to itself; in other words, when all members of the metapopulation adopt the ESS, each individual maximizes its fitness by adopting the ESS, and those that employ a variant strategy do not achieve higher fitness. Consequently, when the metapopulation is not at an ESS, rare variants adopting different persister strategies can invade, and when the majority of individuals adopt the ESS, no other persister strategy can invade from rarity. In Appendix S1, we calculate how persister strategies relate to growth and survival through catastrophe events, and hence Darwinian fitness, and arrive at an implicit solution for the ESS:(1)This can be solved explicitly for numerical parameter values (Figure 2). The same procedure can be used to derive numerical solutions for the extended models incorporating random waiting times until catastrophe (Appendix S1, and Figure 3), less extreme differences between persister and nonpersister cells in their growth or survival rates, and differences in the competitive strain that they exert upon the population's resources (Appendix S1, and Figure 4).

Bottom Line: Persistence has a direct benefit to cells because it allows survival during catastrophes-a form of bet-hedging.However, persistence can also provide an indirect benefit to other individuals, because the reduced growth rate can reduce competition for limiting resources.More generally, our results clarify the links between persistence and other bet-hedging or social behaviours.

View Article: PubMed Central - PubMed

Affiliation: St John's College, Oxford University, Oxford, United Kingdom. andy.gardner@ed.ac.uk

ABSTRACT
The ability of bacteria to evolve resistance to antibiotics has been much reported in recent years. It is less well-known that within populations of bacteria there are cells which are resistant due to a non-inherited phenotypic switch to a slow-growing state. Although such 'persister' cells are receiving increasing attention, the evolutionary forces involved have been relatively ignored. Persistence has a direct benefit to cells because it allows survival during catastrophes-a form of bet-hedging. However, persistence can also provide an indirect benefit to other individuals, because the reduced growth rate can reduce competition for limiting resources. This raises the possibility that persistence is a social trait, which can be influenced by kin selection. We develop a theoretical model to investigate the social consequences of persistence. We predict that selection for persistence is increased when: (a) cells are related (e.g. a single, clonal lineage); and (b) resources are scarce. Our model allows us to predict how the level of persistence should vary with time, across populations, in response to intervention strategies and the level of competition. More generally, our results clarify the links between persistence and other bet-hedging or social behaviours.

Show MeSH
Related in: MedlinePlus