Differential Gene Expression Correlates with Behavioural Polymorphism during Collective Behaviour in Cockroaches

SIMPLE SUMMARY: It is currently well accepted that animals differ from one another in their behaviour and tendency to perform actions, a property we refer to as animal personality. In group-living animals, variation in animal personality can be important to determine group survival, as it determines how individuals interact with each other and with their environment. However, we have little knowledge of the proximal mechanisms underlying personality, particularly in group-living organisms. Here, we investigate the relationship between gene expression and two behavioural types (bold and shy) in a gregarious species: the American cockroach. Our results show that bold individuals have upregulated genes with functions associated with sensory activity (phototaxis and odour detection) and aggressive/dominant behaviour, and suggest that social context can modulate gene expression related to bold/shy characteristics. This work could help identify genes important in the earliest stages of group living and social life, and provides a first step toward establishing cockroaches as a focal group for the study of the evolution of sociality. ABSTRACT: Consistent inter-individual variation in the propensity to perform different tasks (animal personality) can contribute significantly to the success of group-living organisms. The distribution of different personalities in a group influences collective actions and therefore how these organisms interact with their environment. However, we have little understanding of the proximate mechanisms underlying animal personality in animal groups, and research on this theme has often been biased towards organisms with advanced social systems. The goal of this study is to investigate the mechanistic basis for personality variation during collective behaviour in a species with rudimentary societies: the American cockroach. We thus use an approach which combines experimental classification of individuals into behavioural phenotypes (‘bold’ and ‘shy’ individuals) with comparative gene expression. Our analyses reveal differences in gene expression between behavioural phenotypes and suggest that social context may modulate gene expression related to bold/shy characteristics. We also discuss how cockroaches could be a valuable model for the study of genetic mechanisms underlying the early steps in the evolution of social behaviour and social complexity. This study provides a first step towards a better understanding of the molecular mechanisms associated with differences in boldness and behavioural plasticity in these organisms.