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.
These cells are sometimes called persister cells, because they are able to persist in the face of catastrophic events such as antibiotic treatment. In the case of antibiotic treatment, persister cells are able to survive because an important action of antibiotics relies on disrupting translation of the mRNA code to polypeptide chains, and this process does not occur in non-growing cells.
A key aspect of persister cells is that their resistance to antibiotic treatment is not genetically determined. Consequently, following antibiotic treatment, persisters give rise to new populations that have the same vulnerability to antibiotic treatment as the ancestral population. The resistance of persister cells is therefore determined phenotypically, with cells switching between the alternative phenotypic states of persistence and normal growth.
Although much effort has gone into understanding the mechanistics of persistence, little attention has been given to the evolutionary forces that explain why persistence should be favoured. The prevalent view within the microbial literature is that this behaviour can explained by benefits accruing at the level of the population, since persister cells represent an insurance policy that permits population survival in the event of catastrophe.
However, the idea that traits are favoured because they benefit the population was generally rejected in the evolutionary literature by a large body of theoretical and empirical work instigated in the 1960s. Instead, it is necessary to consider the costs and benefits of a trait, both for the individual that performs it, and for those that they interact with. Persistence has a direct benefit to cells because it allows survival during catastrophes. In this respect it can be compared with other bet-hedging strategies such as seed dormancy and insect diapause.
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 problem that cells that allocate more time to the persister state could be out-competed by cells which allocate less time to the persister state, and instead invest more heavily in growth. We develop a theoretical model that makes explicit the direct (selfish) and indirect (social) fitness consequences of persistence.
This allows us to predict how the evolutionary stable level of persisters depends upon population demographic parameters such as intensity of resource competition, the frequency of catastrophes such as antibiotic treatment, and the genetic structure (heterogeneity) of populations. Our model allows us to investigate the evolutionary conflict (tension) between the interests of the individual, and that of the group or population. This clarifies links to other microbial social traits, as well as organisms that are more often studied from a social perspective such as ants, and other social animals.