Competitive fates of bacterial social parasites: persistence and self–induced extinction ofMyxococcus xanthuscheaters

Abstract

Cooperative biological systems are susceptible to disruption by cheating. Using the social bacterium Myxococcus xanthus, we have tested the short-term competitive fates of mixed cheater and wild-type strains over multiple cycles of cooperative development. Cheater/wild-type mixes underwent several cycles of starvation-induced multicellular development followed by spore germination and vegetative population growth. The population sizes of cheater and wild-type strains in each pairwise mixture were measured at the end of each developmental phase and each growth phase. Cheater genotypes showed several distinct competitive fates, including cheater persistence at high frequencies with little effect on total population dynamics, cheater persistence after major disruption of total population dynamics, self-extinction of cheaters with wild-type survival, and total population extinction. Our results empirically demonstrate that social exploitation can destabilize a cooperative biological system and increase the risk of local extinction events.

Group-beneficial traits, frequency-dependent selection and genotypic diversity: an antibiotic resistance paradigm

“…Velicer and colleagues (Velicer et al 1998(Velicer et al , 2000Velicer & Stredwick 2002;Fiegna & Velicer 2003;Velicer & Yu 2003) and Strassmann and colleagues (Strassmann et al 2000;Foster et al 2002;Fortunato et al 2003a,b;Queller et al 2003) have shown that cheaters may be common in the bacterium Myxococcus xanthus and in the social amoeba, Dictyostelium discoideum, respectively. In these cases, when the organisms are starved they amass into a non-migrating fruiting body or a slug, respectively, and cheater clones make up a small fraction of stalk-like reproductive structures.…”

What can microbial genetics teach sociobiology?

“…Similarly, strains of the pathogenic bacterium Pseudomonas aeruginosa that do not produce the siderophores that are required to scavenge insoluble iron from the environment [33,34] also fare better than wild-type cells in mixtures. In addition, in societies of the bacterium Myxococcus xanthus [19,[35][36][37] and the slime mold Dictyostelium discoideum [38], mutants have been identified that overproduce spores at the expense of other strains in the fruiting body. The ability to generate these strains is of great importance, because it shows that crude genetic changes, including whole-gene knockouts, can result in exploitative behaviors that threaten social groups.…”

“…have reduced fitness) [10][11][12][13][14][15]. It seems probable that the failure of certain cheater alleles of D. discoideum [38] and M. xanthus [19,[35][36][37] to spread might be similarly explained. Therefore, the ability to create cheater mutants has provided unique and powerful ways to test a central prediction of sociobiology: that relatedness promotes cooperation [3,11].…”

“…Therefore, the ability to create cheater mutants has provided unique and powerful ways to test a central prediction of sociobiology: that relatedness promotes cooperation [3,11]. These and other studies have provided experimental confirmation of the idea that cheaters only succeed under conditions in which individuals are not highly related [19,[33][34][35]38].…”

Chimaeric load among sympatric social bacteria increases with genotype richness

“…Genetically distinct conspecific cells will co-occur in chimaeric local groups due to mutation and possibly migration, and are likely to interact in ways that affect fitness [9,18,19]. Such intra-specific interactions may promote or diminish genetic diversity [20] and may even affect the persistence of whole populations [21]. If interactions among neighbours that are likely to encounter one another are predominantly negative, then the resulting chimaeric load is expected to increase selection for mechanisms to prevent co-aggregation of distinct genotypes into common social groups.…”