Evolution of an obligate social cheater to a superior cooperator

Abstract

Obligate relationships have evolved many times and can be parasitic or mutualistic. Obligate organisms rely on others to survive and thus coevolve with their host or partner. An important but little explored question is whether obligate status is an evolutionarily terminal condition or whether obligate lineages can evolve back to an autonomous lifestyle. The bacterium Myxococcus xanthus survives starvation by the social development of spore-bearing fruiting bodies. Some M. xanthus genotypes defective at fruiting body development in isolation can nonetheless exploit proficient genotypes in chimaeric groups. Here we report an evolutionary transition from obligate dependence on an altruistic host to an autonomous mode of social cooperation. This restoration of social independence was caused by a single mutation of large effect that confers fitness superiority over both ancestral genotypes, including immunity from exploitation by the ancestral cheater. Thus, a temporary state of obligate cheating served as an evolutionary stepping-stone to a novel state of autonomous social dominance.

What can microbial genetics teach sociobiology?

“…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].…”

“…The use of microorganisms offers a possible solution, because microorganisms can be made to evolve in the laboratory and adaptation followed as it occurs, with the potential for identifying the causal genetic changes. The elegance of this approach was recently shown by an experimental evolution study of the bacterium M. xanthus [19,37], which, similar to D. discoideum, forms fruiting bodies on starvation ( Figure 1c,d). Cheater mutants were pitted against wild-type cells in mixed groups over multiple cycles of fruiting-body formation.…”

“…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].…”

“…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.…”

“…For example, many microorganisms share molecules that are secreted into the environment, including enzymes that break down food, quorum-sensing signals, siderophores (which scavenge iron) and the protective polymeric slime that is released in bacterial biofilms [10][11][12][13][14][15]17] (Figure 1a,b). There is more sophisticated sociality too: this is epitomized by the dictyostelid amebae [18] and the Myxobacteria (also known as Myxococcales) [19], in both of which cells aggregate and many cells die so that others can be propagated as spores in terminally differentiated fruiting bodies (Figure 1c,d). Crucially, such traits have the potential for 'cheaters' to gain a selfish advantage by using the resources of others without themselves paying the full cost.…”