Conflict of interest and signal interference lead to the breakdown of honest signaling

Abstract

Animals use signals to coordinate a wide range of behaviors, from feeding offspring to predator avoidance. This poses an evolutionary problem, because individuals could potentially signal dishonestly to coerce others into behaving in ways that benefit the signaler. Theory suggests that honest signaling is favored when individuals share a common interest and signals carry reliable information. Here, we exploit the opportunities offered by bacterial signaling to test these predictions with an experimental evolution approach. We show that: (1) reduced relatedness leads to the relative breakdown of signaling, (2) signaling breaks down by the invasion of mutants that show both reduced signaling and reduced response to signal, (3) the genetic route to signaling breakdown is variable, and (4) the addition of artificial signal, to interfere with signal information, also leads to reduced signaling. Our results provide clear support for signaling theory, but we did not find evidence for previously predicted coercion at intermediate relatedness, suggesting that mechanistic details can alter the qualitative nature of specific predictions. Furthermore, populations evolved under low relatedness caused less mortality to insect hosts, showing how signal evolution in bacterial pathogens can drive the evolution of virulence in the opposite direction to that often predicted by theory.

The Fitness of Pseudomonas aeruginosa Quorum Sensing Signal Cheats Is Influenced by the Diffusivity of the Environment

“…Our work opens up new avenues for exploring how, when, and why bacterial signaling evolves in different environments and why we find a variety of QS mutant genotypes and phenotypes in natural environments (8–14, 38, 39). P. aeruginosa clones carrying mutations in the lasI (3O-C 12 -HSL) and rhll (C 4 -HSL) QS signals have been isolated from chronically infected cystic fibrosis patients and mechanically ventilated hospital patients (8–11).…”

The evolutionary ecology of molecular replicators

“…Finally, we see this work as squarely fitting into the emerging field known as sociomicrobiology, which has enjoyed increasing success in fusing contemporary social evolution theory with expanding knowledge of the biological behavioural repertoire of bacteria [72]. The analysis presented in this paper simply includes even more minute entities into this discipline and the title could refer to sociomicrobiology instead of behavioural ecology, the latter simply coined to free the study of sociobiology from its political contaminants [73].…”

Combinatorial quorum sensing in Pseudomonas aeruginosa allows for novel cheating strategies

“…Social traits and sociality in bacteria have received extensive attention in recent years, from the exploitation of collective behaviors by cheats [1][2][3][4][5][6][7][8][9][10], to the implications for infection [6,11,12]. Pseudomonas aeruginosa lasR quorum sensing (QS) mutants have previously been shown to act as social cheats in environments where QS is required for growth.…”

“…QS lasR mutants are also frequently isolated from cystic fibrosis (CF) lungs [14,15], and they readily arise during longterm selection experiments where the QS controlled production of public goods can be easily exploited [3,16]. More recently, QS signals themselves have been shown to be exploitable by lasI signal cheats in specific environments [7].…”