Cooperation and division of labour are fundamental in the 'major transitions' in evolution. While the factors regulating cell differentiation in multi-cellular organisms are quite well understood, we are just beginning to unveil the mechanisms underlying individual specialization in cooperative groups of animals. Clonal ants allow the study of which factors influence task allocation without confounding variation in genotype and morphology. Here, we subjected larvae and freshly hatched workers of the clonal ant to different rearing conditions and investigated how these manipulations affected division of labour among pairs of oppositely treated, same-aged clonemates. High rearing temperature, physical stress, injury and malnutrition increased the propensity of individuals to become subordinate foragers rather than dominant reproductives. This is reflected in changed gene regulation: early stages of division of labour were associated with different expression of genes involved in nutrient signalling pathways, metabolism and the phenotypic response to environmental stimuli. Many of these genes appear to be capable of responding to a broad range of stressors. They might link environmental stimuli to behavioural and phenotypic changes and could therefore be more broadly involved in caste differentiation in social insects. Our experiments also shed light on the causes of behavioural variation among genetically identical individuals.
The fat body, a major metabolic hub in insects, is involved in many functions, e.g. energy storage, nutrient sensing and immune response. In social insects, fat appears to play an additional role in division of labour between egg layers and workers, which specialize in nonreproductive tasks inside and outside their nest. For instance, reproductives are more resistant to starvation, and changes in fat content have been associated with the transition from inside to outside work or reproductive activities. However, most studies have been correlative and we still need to unravel the causal interrelationships between fat content and division of both reproductive and nonreproductive labour. Clonal ants, e.g. Platythyrea punctata, are ideal models for studying task partitioning without confounding variation in genotype and morphology. In this study, we examined the range of variation and flexibility of fat content throughout the lifespan of workers, the threshold of corpulence associated with foraging or reproduction and whether low fat content is a cause rather than a consequence of the transition to foraging. We found that lipid stores change with division of labour from corpulent to lean and, in reverted nurses, back to corpulent. In addition, our data show the presence of fat content thresholds that trigger the onset of foraging or egg-laying behaviour. Our study supports the view that mechanisms that regulate reproduction and foraging in solitary insects, in particular the nutritional status of individuals, have been co-opted to regulate division of labour in colonies of social insects.
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