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...

Kin recognition helps cooperation to evolve in many animals, but it is uncertain whether microorganisms can also use it to focus altruistic behaviour on relatives. Here we show that the social amoeba Dictyostelium purpureum prefers to form groups with its own kin in situations where some individuals die to assist others. By directing altruism towards kin, D. purpureum should generally avoid the costs of chimaerism experienced by the related D. discoideum.

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A major problem in evolutionary biology is explaining the success of mutualism. solving this problem requires understanding the level of fidelity between interacting partners. Recent studies have proposed that fungus-growing ants and their fungal cultivars are the products of 'diffuse' coevolution, in which single ant and fungal species are not exclusive to one another. Here we show for ants and associated fungi in the Cyphomyrmex wheeleri species group that each ant species has been exclusively associated with a single fungal cultivar 'species' for millions of years, even though alternative cultivars are readily available, and that rare shifts to new cultivars are associated with ant speciation. such long-term partner fidelity may have facilitated 'tight' ant-fungus coevolution, and shifts to new fungal cultivars may have had a role in the origin of new ant species.

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The red imported re ant is becoming a global ecological problem, having invaded the United States, Puerto Rico, New Zealand and, most recently, Australia. In its established areas, this pest is devastating natural biodiversity. Early attempts to halt re ant expansion with pesticides actually enhanced its spread. Phorid y parasitoids from South America have now been introduced into the United States as potential biological control agents of the red imported re ant, but the impact of these ies on re ant populations is currently unknown. In the laboratory, we show that an average phorid density of as little as one attacking y per 200 foraging ants decreased colony protein consumption nearly twofold and signi cantly reduced numbers of large-sized workers 50 days later. The high impact of a single phorid occurred mainly because ants decreased foraging rates in the presence of the ies. Our experiments, the rst (to our knowledge) to link indirect and direct effects of phorids on re ants, demonstrate that colonies can be stressed with surprisingly low parasitoid densities. We interpret our ndings with regard to the more complex re antphorid interactions in the eld.

Little is known about the population structure of social microorganisms, yet such studies are particularly interesting for the ways that genetic variation impacts their social evolution. Dictyostelium, a eukaryotic microbe widely used as a developmental model, has a social fruiting stage in which some formerly independent individuals die to help others. To assess genetic variation within the social amoeba Dictyostelium purpureum, we sequenced ~4000 base pairs of ribosomal DNA (rDNA) from 37 isolates collected in Texas, Virginia, and Japan. Our analysis showed extensive genetic variation between populations and clear evidence of phylogenetic structure. We identified three major phylogenetic groups that were more different than other accepted species pairs. Tests using pairs of clones showed that both sexual macrocyst and asexual fruiting body formation were influenced by genetic divergence. Macrocysts were less likely to form between pairs of clones from different groups than from the same group. There was also a correlation between the genetic divergence of a pair of clones and their degree of mixing within fruiting bodies. These observations suggest that cryptic species might occur within D. purpureum and, more importantly, reveal how genetic variation impacts social interactions.

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