Programmed cell death as a black queen in microbial communities

Programmed cell death (PCD) in unicellular organisms is in some instances an altruistic trait. When the beneficiaries are clones or close kin, kin selection theory may be used to explain the evolution of the trait, and when the trait evolves in groups of distantly related individuals, group or multilevel selection theory is invoked. In mixed microbial communities, the benefits are also available to unrelated taxa. But the evolutionary ecology of PCD in communities is poorly understood. Few hypotheses have been offered concerning the community role of PCD despite its far-reaching effects. The hypothesis we consider here is that PCD is a black queen. The Black Queen Hypothesis (BQH) outlines how public goods arising from a leaky function are exploited by other taxa in the community. Black Queen (BQ) traits are essential for community survival, but only some members bear the cost of possessing them, while others lose the trait In addition, BQ traits have been defined in terms of adaptive gene loss, and it is unknown whether this has occurred for PCD. Our conclusion is that PCD fulfils the two most important criteria of a BQ (leakiness and costliness), but that more empirical data are needed for assessing the remaining two criteria. In addition, we hold that for viewing PCD as a BQ, the original BQH needs to include social traits. Thus, despite some empirical and conceptual shortcomings, the BQH provides a helpful avenue for investigating PCD in microbial communities.

Automated summary

Programmed cell death (PCD) in unicellular organisms can be seen as an altruistic trait, possibly explained by kin selection or group selection theory. The Black Queen Hypothesis (BQH) suggests that PCD functions as a black queen in microbial communities, with leakiness and costliness being key characteristics. More empirical data is needed to fully assess this hypothesis, but it provides a useful framework for studying the role of PCD in communities.