Kin discrimination and cooperation in microbes.

Recognition of relatives is important in microbes because they perform many behaviors that have costs to the actor while benefiting neighbors. Microbes cooperate for nourishment, movement, virulence, iron acquisition, protection, quorum sensing, and production of multicellular biofilms or fruiting bodies. Helping others is evolutionarily favored if it benefits others who share genes for helping, as specified by kin selection theory. If microbes generally find themselves in clonal patches, then no special means of discrimination is necessary. Much real discrimination is actually of kinds, not kin, as in poison-antidote systems, such as bacteriocins, in which cells benefit their own kind by poisoning others, and in adhesion systems, in which cells of the same kind bind together. These behaviors can elevate kinship generally and make cooperation easier to evolve and maintain.

Histocompatibility as adaptive response to discriminatory within-organism conflict: a historical model.

Multicellular tissue compatibility, or histocompatibility, restricts fusion to close kin. Histocompatibility depends on hypervariable cue genes, which often have more than 100 alleles in a population. To explain the evolution of histocompatibility, I here take a historical approach. I focus on the specific example of marine invertebrate histocompatibility. I use simple game-theoretical models to show that histocompatibility can evolve through five steps. These steps include the evolution of indiscriminate fusion, the evolution of discriminatory within-organism conflict, the evolution of minor histocompatibility, the evolution of major histocompatibility, and the evolution of major histocompatibility cue polymorphism. Allowing for gradual evolution reveals discriminatory within-organism conflict as a selective pressure for histocompatibility and associated cue polymorphism. Existing data from marine invertebrates and other organisms are consistent with this hypothesis.

High relatedness in a social amoeba: the role of kin-discriminatory segregation.

A major challenge for social theory is to explain the importance of kin discrimination for the evolution of altruism. One way to assess the importance of kin discrimination is to test its effects on increasing relatedness within groups. The social amoeba Dictyostelium discoideum aggregates to form a fruiting body composed of dead stalk and live spores. Previous studies of a natural population showed that where D. discoideum occurs in the soil, multiple clones are often found in the same small soil samples. However, actual fruiting bodies usually contain only one clone. We here performed experiments to gauge the effect of kin-discriminatory segregation on increasing relatedness. We mixed co-occurring clones from this population using a relatedness level found in small soil samples. We found a lower proportion of uniclonal fruiting bodies and a lower level of relatedness compared with natural fruiting bodies. We found that the amount of relatedness increase attributable to kin-discriminatory segregation was small. These findings suggest a relatively minor influence of kin-discriminatory segregation on relatedness in D. discoideum. We discuss our results comparing with the results of previous studies, including those of wild clones and laboratory mutants. We ask why wild clones of D. discoideum exhibit a low degree of kin-discriminatory segregation, and what alternative factors might account for high relatedness in D. discoideum.

Discovery of a large clonal patch of a social amoeba: implications for social evolution.

Studies of genetic population structures of clonally reproducing macro-organisms have revealed large areas where only one clone is found. These areas, referred to as clonal patches, have not been shown to occur in free-living microbes until now. In free-living microbes, high genetic diversity at local scales is usually maintained by high rates of dispersal. We report, however, a highly dense, 12-m clonal patch of the social amoeba Dictyostelium discoideum in a cattle pasture located in a Texas Gulf Coast prairie. We confirm the presence of only one clone by the analysis of 65 samples and amplification of 10 polymorphic microsatellite loci. Samplings of additional cattle pastures nearby showed higher clonal diversity, but with a density of D. discoideum isolates lower than in the clonal patch. These findings show that high rates of microbial dispersal do not always produce genetic diversity at local scales, contrary to the findings of previous studies. The existence of clonal patches may be particularly important for microbial social evolution.

High relatedness maintains multicellular cooperation in a social amoeba by controlling cheater mutants.

The control of cheating is important for understanding major transitions in evolution, from the simplest genes to the most complex societies. Cooperative systems can be ruined if cheaters that lower group productivity are able to spread. Kin-selection theory predicts that high genetic relatedness can limit cheating, because separation of cheaters and cooperators limits opportunities to cheat and promotes selection against low-fitness groups of cheaters. Here, we confirm this prediction for the social amoeba Dictyostelium discoideum; relatedness in natural wild groups is so high that socially destructive cheaters should not spread. We illustrate in the laboratory how high relatedness can control a mutant that would destroy cooperation at low relatedness. Finally, we demonstrate that, as predicted, mutant cheaters do not normally harm cooperation in a natural population. Our findings show how altruism is preserved from the disruptive effects of such mutant cheaters and how exceptionally high relatedness among cells is important in promoting the cooperation that underlies multicellular development.