Evolutionary theory of bacterial quorum sensing: when is a signal not a signal?

Abstract

The term quorum sensing (QS) is used to describe the communication between bacterial cells, whereby a coordinated population response is controlled by diffusible molecules produced by individuals. QS has not only been described between cells of the same species (intraspecies), but also between species (interspecies) and between bacteria and higher organisms (inter-kingdom). The fact that QS-based communication appears to be widespread among microbes is strange, considering that explaining both cooperation and communication are two of the greatest problems in evolutionary biology. From an evolutionary perspective, intraspecies signalling can be explained using models such as kin selection, but when communication is described between species, it is more difficult to explain. It is probable that in many cases this involves QS molecules being used as 'cues' by other species as a guide to future action or as manipulating molecules whereby one species will 'coerce' a response from another. In these cases, the usage of QS molecules cannot be described as signalling. This review seeks to integrate the evolutionary literature on animal signalling with the microbiological literature on QS, and asks whether QS within bacteria is true signalling or whether these molecules are also used as cues or for the coercion of other cells.

Figure 1

Brown and Johnstone's theoretical model of quorum signalling. (a) Cooperation effort increases with increasing relatedness, because the inclusive fitness benefits of cooperation are maximal at high relatedness and minimal at low relatedness. (b) Signalling effort is a dome-shaped function of relatedness, because at low relatedness there is little inclusive fitness benefit to be accrued from organizing a cooperative venture, and at high relatedness there is little conflict so that a cheap signal is favoured, whereas at intermediate relatedness cooperation is worthwhile, yet there is also a scope for conflict, hence a costly signal is required to initiate competition.