Queen Longevity and Fecundity Affect Conflict with Workers over Resource Inheritance in a Social Insect.

Resource inheritance is a major source of conflict in animal societies. However, the assumptions and predictions of models of conflict over resource inheritance have not been systematically tested within a single system. We developed an inclusive fitness model for annual eusocial Hymenoptera that predicts a zone of conflict in which future reproductive workers are selected to enforce nest inheritance before the queen is selected to cede the nest. We experimentally tested key elements of this model in the bumblebee Bombus terrestris. In colonies from which queens were sequentially removed, queen tenure was significantly negatively associated with worker male production, confirming that workers gain direct fitness by usurping the queen. In unmanipulated colonies, queen fecundity decreased significantly over the latter part of the colony cycle, confirming that workers' indirect fitness from maintaining queens declines over time. Finally, in an experiment simulating loss of queen fecundity by removal of queens' eggs, worker-to-queen aggression increased significantly and aggressive workers were significantly more likely to become egg layers, consistent with workers monitoring queen fecundity to assess the net benefit of future reproduction. Overall, by upholding key assumptions and predictions of the model, our results provide novel empirical support for kin-selected conflict over resource inheritance.

Evolution of ageing, costs of reproduction and the fecundity-longevity trade-off in eusocial insects.

Eusocial insects provide special opportunities to elucidate the evolution of ageing as queens have apparently evaded costs of reproduction and reversed the fecundity-longevity trade-off generally observed in non-social organisms. But how reproduction affects longevity in eusocial insects has rarely been tested experimentally. In this study, we took advantage of the reproductive plasticity of workers to test the causal role of reproduction in determining longevity in eusocial insects. Using the eusocial bumblebee Bombus terrestris, we found that, in whole colonies, in which workers could freely 'choose' whether to become reproductive, workers' level of ovarian activation was significantly positively associated with longevity and ovary-active workers significantly outlived ovary-inactive workers. By contrast, when reproductivity was experimentally induced in randomly selected workers, thereby decoupling it from other traits, workers' level of ovarian activation was significantly negatively associated with longevity and ovary-active workers were significantly less long-lived than ovary-inactive workers. These findings show that workers experience costs of reproduction and suggest that intrinsically high-quality individuals can overcome these costs. They also raise the possibility that eusocial insect queens exhibit condition-dependent longevity and hence call into question whether eusociality entails a truly reversed fecundity-longevity trade-off involving a fundamental remodelling of conserved genetic and endocrine networks underpinning ageing.

Gene expression differences in relation to age and social environment in queen and worker bumble bees.

Eusocial insects provide special insights into the genetic pathways influencing aging because of their long-lived queens and flexible aging schedules. Using qRT-PCR in the primitively eusocial bumble bee Bombus terrestris (Linnaeus), we investigated expression levels of four candidate genes associated with taxonomically widespread age-related pathways (coenzyme Q biosynthesis protein 7, COQ7; DNA methyltransferase 3, Dnmt3; foraging, for; and vitellogenin, vg). In Experiment 1, we tested how expression changes with queen relative age and productivity. We found a significant age-related increase in COQ7 expression in queen ovary. In brain, all four genes showed higher expression with increasing female (queen plus worker) production, with this relationship strengthening as queen age increased, suggesting a link with the positive association of fecundity and longevity found in eusocial insect queens. In Experiment 2, we tested effects of relative age and social environment (worker removal) in foundress queens and effects of age and reproductive status in workers. In this experiment, workerless queens showed significantly higher for expression in brain, as predicted if downregulation of for is associated with the cessation of foraging by foundress queens following worker emergence. Workers showed a significant age-related increase in Dnmt3 expression in fat body, suggesting a novel association between aging and methylation in B. terrestris. Ovary activation was associated with significantly higher vg expression in fat body and, in younger workers, in brain, consistent with vitellogenin's ancestral role in regulating egg production. Overall, our findings reveal a mixture of novel and conserved features in age-related genetic pathways under primitive eusociality.