Chimeric Synergy in Natural Social Groups of a Cooperative Microbe

Many cooperative species form internally diverse social groups in which individual fitness depends significantly on group-level productivity from cooperation [1-4]. For such species, selection is expected to often disfavor within-group diversity that reduces cooperative productivity [5, 6]. While diversity within social groups is known to enhance productivity in some animals [7-9], diversity within natural groups of social microbes is largely unexamined in this regard. Cells of the soil bacterium Myxococcus xanthus respond to starvation by constructing multicellular fruiting bodies within each of which a subpopulation of cells transforms into stress-resistant spores [10]. Fruiting bodies isolated from soil often harbor substantial endemic diversity [11] that is, nonetheless, lower than between-group diversity, which increases with distance from millimeter to global scales [12-14]. We show that M. xanthus clones isolated from the same fruiting body often collectively produce more viable spores in chimeric groups than expected from sporulation in genetically homogeneous groups. In contrast, chimerism among clones derived from different fruiting bodies tends to reduce group productivity, and it does so increasingly as a function of spatial distance between fruiting-body sample sites. For one fruiting body examined in detail, chimeric synergy-a positive quantitative effect of chimerism on group productivity-is distributed broadly across an interaction network rather than limited to a few interactions. We propose that these results strengthen the plausibility of the hypothesis that selection may operate not only within Myxococcus groups, but also between kin groups to disfavor within-group variation that reduces productivity while allowing some forms of diversity that generate chimeric synergy to persist.