Specialisation and plasticity in a primitively social insect

Abstract Biological systems not only have the remarkable capacity to build and maintain complex spatio-temporal structures in noisy environments, they can also rapidly break up and rebuild such structures. How such systems can simultaneously achieve both robust specialisation and plasticity is poorly understood. Here we use primitive societies of Polistes wasps as a model system where we experimentally perturb the social structure by removing the queen and follow the re-establishment of the social steady state over time. We combine a unique experimental strategy correlating time-resolved measurements across vastly different scales with a theoretical approach. We show that Polistes integrates antagonistic processes on multiple scales to distinguish between extrinsic and intrinsic perturbations and thereby achieve both robust specialisation and rapid plasticity. The long-term stability of the social structure relies on dynamic DNA methylation which controls transcriptional noise. Such dynamics provide a general principle of how both specialization and plasticity can be achieved in biological systems. One Sentence SummaryA primitive social insect simultaneously achieves specialisation and plasticity by integrating antagonistic dynamics on different scales. HighlightsWe employ a unique experimental approach correlating dynamics of societies, individuals, and epigenetic gene regulationA social insect simultaneously achieves specialisation and plasticity by integrating antagonistic processes on different spatial scalesRegulation of population-level noise by DNA methylation ensures long-term stability of phenotypic specialisation