Selection favors incompatible signaling in bacteria.

A cooperative group can achieve more than the sum of its members. Evolution has taken advantage of this principle in most natural systems, from multicellular individuals to ant colonies. To do so, it has provided the members of cooperative groups with communication tools, which are critical for effective cooperation. For example, some ants form bridges with their bodies to help their nest-mates cross a gap (1, 2). But this admirable behavior only makes sense when many ants mass along the same route; a lone scout that stayed put across a gap instead of wandering off in search for food would do a disservice to the colony. Similarly, many bacteria cooperate in ways that only make sense in large groups, for example secreting a sticky goo to keep bacteria together forming a biofilm, or a slippery one to help movement (3). To prevent wasting resources on these public goods when bacterial density is too low to have an advantage from them,many species measure local bacterial density using a mechanism called quorum sensing, and produce the public good only when numbers are high enough to make it count (4). This function of quorum sensing seems straightforward, but one piece of information does not quite make sense: in natural populations, different individuals have different—and incompatible—quorumsensing machineries (5). If the bacteria are trying to coordinatewith their neighbors, why do they use a different signaling system? In PNAS, Pollak et al. demonstrate an elegant answer to this question: a rare mutant with incompatible quorum-sensing machinery initially exploits the wild-type, but is able to cooperate with its own kind when common in the population (6). Quorum sensing is elegantly simple. The bacterium produces an autoinducer molecule that activates the cooperative mechanism. Unlike regular activation mechanisms, however, the autoinducer molecule does not stay inside the bacterium, but is instead secreted to the environment. If few bacteria are present, the autoinducer will diffuse away faster than it is produced, and the local concentration will be too low to activate cooperation. In contrast, a dense group of bacteria will accumulate enough autoinducer, triggering cooperation precisely when coordinated behavior is most effective (Fig. 1A) (4). Similar to many other cooperative schemes, however, quorum sensing is vulnerable to cheaters (7). A mutant invader that ignores the autoinducer will benefit from the public good produced by cooperators, without contributing anything. The cheating mutant will grow faster than the wild-type, growing in frequency and hindering cooperation, so the population will grow more slowly (Fig. 1B). In a paper published in PNAS in 2011, Avigdor Eldar predicted a different fate for an invader that carries an incompatible quorum-sensing machinery Fig. 1. Facultative cheating promotes the coexistence of different quorumsensing mechanisms. (A) Growth of a population with a single strain of quorumsensing bacteria (arrows represent time): at low frequencies, autoinducer concentration is too low to trigger the cooperative production of a public good (Left). When density is high enough, cooperation starts (Center). Cooperation benefits the group, allowing fast growth of the community up to high densities (Right). (B) Same as A, but in a mixed population with some cheater cells that do not respond to the autoinducer (red). Cheaters benefit from the public good produced by cooperators without contributing, thus growing in frequency. Because fewer cells contribute to the public good, the population growsmore slowly than a pure culture of cooperators. (C) Same as A, but in mixed populations with two different strains of quorum-sensing bacteria (each strain responds only to its own autoinducer). (Upper) Starting condition with a minority of green cells. (Lower) Starting condition with a minority of blue cells. Both starting conditions lead to the same qualitative outcome: the minority strain acts as a cheater for some time, but eventually both strains reach enough density to trigger cooperation, and the population grows fast. (D) Fitness of each strain as a function of their relative frequency. Facultative cheating produces negative frequency-dependent selection (each strain has fitness advantage when at low frequency), leading to stable coexistence.