Abstract
How does metabolism influence social behavior? This fundamental question at the interface of molecular biology and social evolution is hard to address with experiments in animals, and therefore, we turned to a simple microbial system: swarming in the bacterium Pseudomonas aeruginosa. Using genetic engineering, we excised a locus encoding a key metabolic regulator and disrupted P. aeruginosa’s metabolic prudence, the regulatory mechanism that controls expression of swarming public goods and protects this social behavior from exploitation by cheaters. Then, using experimental evolution, we followed the joint evolution of the genome, the metabolome and the social behavior as swarming re-evolved. New variants emerged spontaneously with mutations that reorganized the metabolome and compensated in distinct ways for the disrupted metabolic prudence. These experiments with a unicellular organism provide a detailed view of how metabolism—currency of all physiological processes—can determine the costs and benefits of a social behavior and ultimately influence how an organism behaves towards other organisms of the same species.
Highlights
Metabolism influences the way individuals behave toward others
Since metabolism is the currency of all physiological processes that support life (Smith and Morowitz 2004) and a major determinant of behavioral cost (Biro and Stamps 2010), natural selection should favor a regulation of social behavior that reduces metabolic burden on the actor
Excision at cbrA Locus Disrupts Metabolic Prudence and Produces a Synthetic Altruist Swarming is a social behavior that relies on the collective secretion of rhamnolipid surfactants; metabolic prudence regulates expression of the rhlA gene for rhamnolipid synthesis, ensuring that P. aeruginosa produces these surfactant public goods only when it has carbon available in excess relative to other nutrients such as nitrogen
Summary
Metabolism influences the way individuals behave toward others. In all species, from bacteria to animals including humans, social behavior appears to be a function of metabolic state (Robinson et al 2008; Biro and Stamps 2010; Boyle et al 2015; Sih et al 2015). Vampire bats share blood with their starving roost-mates, but they share more when they have fed well (Carter and Wilkinson 2013); bacteria send and receive more chemical quorum-sensing signals to one another when they have more intracellular metabolites (Xavier and Bassler 2005); and judges give more favorable parole decisions when they resume their work after a meal (Danziger et al 2011). Why is it that—across the tree of life— metabolism seems to condition social behavior?. Since metabolism is the currency of all physiological processes that support life (Smith and Morowitz 2004) and a major determinant of behavioral cost (Biro and Stamps 2010), natural selection should favor a regulation of social behavior that reduces metabolic burden on the actor
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