More than 50 years after William Hamilton laid the mathematical foundations of kin-selection theory, how cooperation among genetically distinct individuals evolves and is maintained remains one of the most fundamental and fascinating themes of evolutionary research. Of particular importance to this broad theme is the question of how genetic and behavioural diversity within cooperative groups affects group productivity when the latter is a major component of group-member fitness.
Among animals, examples of within-group behavioural diversity that increase total group cooperative productivity abound. However, although research on microbial social evolution has burgeoned in the past two decades, no study has addressed whether cooperative microbes similarly evolve genetic diversity within natural social groups that increases group productivity. Hence, we tested the effects of natural diversity within fruiting bodies of the social bacterium Myxococcus xanthus on total group spore productivity.
This study demonstrates the first examples of chimeric synergy - i.e. positive effects of social chimerism on total group productivity - among conspecific microbes derived from the same natural social group. Moreover, the “social network” within one set of isolates derived from the same fruiting body were also examined in great detail. These analyses show that the chimeric synergy generated by interaction among the distinct members of this fruiting-body group is broadly distributed across genotypes and interactions rather than being (less interestingly) due to social responses by one genotype or a small minority of genotypes.
Interestingly, the chimeric synergy occurs almost exclusively among M. xanthus isolates derived from the same fruiting body. In contrast, forced chimerism among isolates derived from different fruiting bodies generates almost exclusively strongly negative effects on group productivity (chimeric load). Thus, this study not only document naturally evolved, within-group chimeric synergy among microbes, but also the stark dichotomy of such positive within-group interactions to pervasive between-group antagonism, a dichotomy common among cooperative animal species.
These observations therefore suggest both i) that group-level performance during fruiting body development is a major component of fitness for M. xanthus cells and ii) that such selection can operate to maintain within-group diversity of positive effect on group-level performance while purging within-group diversity of negative effect. These results also reveal the absence of selection for divergent lineages across groups to remain socially compatible, thus leading to the quantitative decay of cooperation as a function of spatial distance between isolate origins (and hence as a function of genetic distance between isolates) in experimental between-group chimeras. Thus, the findings from this study are consistent with an intuitively appealing model of selection operating at multiple levels of biological organization in natural populations of bacteria, with selection among higher-level units (in this case fruiting-body-forming groups) being strong enough to differentiate the fundamental social character of within-group versus between-group genetic variation.