A Simple Mechanism for Complex Social Behavior

Video: Dictyostelium discoideum (social amoeba): film of slime moulds by Professor John Bonner of Princeton University.

Cells' life and death decisions: lessons from a social amoeba
Life is full of choices, not only for people but also for the cells that we're made of. Scientists in Manchester are studying a simple life form to uncover the basis of cells' choices, as Michael Regnier reports.
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Reference
A Simple Mechanism for Complex Social Behavior
PLoS Biol 9(3): e1001039. doi:10.1371/journal.pbio.1001039
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Abstract
The evolution of cooperation is a paradox because natural selection should favor exploitative individuals that avoid paying their fair share of any costs. Such conflict between the self-interests of cooperating individuals often results in the evolution of complex, opponent-specific, social strategies and counterstrategies. However, the genetic and biological mechanisms underlying complex social strategies, and therefore the evolution of cooperative behavior, are largely unknown. To address this dearth of empirical data, we combine mathematical modeling, molecular genetic, and developmental approaches to test whether variation in the production of and response to social signals is sufficient to generate the complex partner-specific social success seen in the social amoeba Dictyostelium discoideum. Firstly, we find that the simple model of production of and response to social signals can generate the sort of apparent complex changes in social behavior seen in this system, without the need for partner recognition. Secondly, measurements of signal production and response in a mutant with a change in a single gene that leads to a shift in social behavior provide support for this model. Finally, these simple measurements of social signaling can also explain complex patterns of variation in social behavior generated by the natural genetic diversity found in isolates collected from the wild. Our studies therefore demonstrate a novel and elegantly simple underlying mechanistic basis for natural variation in complex social strategies in D. discoideum. More generally, they suggest that simple rules governing interactions between individuals can be sufficient to generate a diverse array of outcomes that appear complex and unpredictable when those rules are unknown.

Author Summary
Despite the appearance of cooperation in nature, selection should often favor exploitative individuals who perform less of any cooperative behaviors while maintaining the benefits accrued from the cooperative behavior of others. This conflict of interest among cooperating individuals can lead to the evolution of complex social strategies that depend on the identity (e.g. genotype or strategy) of the individuals with whom you interact. The social amoeba Dictyostelium discoideum provides a compelling model for studying such "partner specific" conflict and cooperation. Upon starvation, free-living amoebae aggregate and form a fruiting body composed of dead stalk cells and hardy spores. Different genotypes will aggregate to produce chimeric fruiting bodies, resulting in potential social conflict over who will contribute to the reproductive sporehead and who will "sacrifice" themselves to produce the dead stalk. The outcomes of competitive interactions in chimera appear complex, with social success being strongly partner specific. Here we propose a simple mechanism to explain social strategies in D. discoideum, based on the production of and response to stalk-inducing factors, the social signals that determine whether cells become stalk or spore. Indeed, measurements of signal production and response can predict social behavior of different strains, thus demonstrating a novel and elegantly simple underlying mechanistic basis for natural variation in complex facultative social strategies. This suggests that simple social rules can be sufficient to generate a diverse array of behavioral outcomes that appear complex and unpredictable when those rules are unknown.

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