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.ooperation is a hallmark of major transitions in biological complexity: from molecules to genes, from genes to chromosomes, from primitive cells to complex cells, from cells to multicellular organisms, and from multicellular organisms to societies (1-3). Cooperative groups are vulnerable, however, to exploitation by cheaters, individuals that have access to group benefits without contributing their fair share (1-3). Among cells and individuals, high relatedness is thought to aid in selection against cheaters (4-6). High relatedness means that cheaters and cooperators will tend to be in different groups, which both limits opportunities for cheaters to exploit cooperators and exposes any group-level defects of cheaters to selection. Curiously, although such control is central to selfish-gene theory, tests at the genetic level have been limited by the kinds of information available. In large organisms, relatedness is often estimated, but cheater genes are unknown. In microorganisms, cheater genes can be found (7-13), but little is known about relatedness in natural social groups.The life cycle of social amoebae presents a challenge to the importance of relatedness in promoting selection against cheaters and an opportunity to test it. When the normally solitary amoebae are starved of their bacterial food source, they gather into a multicellular aggregate that forms a fruiting body. Here, Ϸ25% of cells altruistically die, forming a stalk that holds up the remaining cells, differentiated as spores, for dispersal (14-17). Thus, unlike more familiar organisms that develop from one cell, development begins by aggregation of many dispersed cells. Different clones can mix and cheat each other (18,19), for example by avoiding contributing to the sterile stalk (7). Models (20)(21)(22), experiments (7,23,24), and a natural observation (24), suggest that cooperative fruiting body formation can be threatened by the spread of mutant cheat...

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.

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.

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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.

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Wang and Lu (1) claim to report evidence of a genetic polymorphism of altruistic and nonaltruistic alleles in a natural population of Tibetan ground tits, Pseudopodoces humilis. Their argument assumes that observed heritable variation in altruistic behavior reflects an underlying genetic difference in altruism. However, the authors do not show genetic evidence of an underlying difference, and there is another interpretation of their results. The observed difference in altruism could be the consequence of a genetic difference in the tendency to join groups, because joining groups is a necessary prerequisite to expressing altruism. Thus, the heritable difference may only be in the tendency to associate, or enter the contexts within which social actions like altruism are usually expressed (2).What Wang and Lu (1) actually measure is how often birds join groups or nest alone. Their claim about altruism rests on the argument that only birds that join nests can "ever" help, while those that do not join never help. However, Wang and Lu do not show that birds that never help lack the genes for altruism. By analogy, one might find that only some chameleons ever turn green, while others never do. However, if some never turn green only because they avoid green foliage, and all chameleons can turn green, the difference in "greenness" would be environmental, not genetic. Similarly, all birds in Wang and Lu's study could be altruistic in the same way, differing only in their propensity to associate.By conflating "altruism" and "association," Wang and Lu ( 1) perpetuate what Hamilton (3) called "one of