Aging- and task-related resilience decline is linked to food responsiveness in highly social honey bees.

Conventional invertebrate models of aging have provided striking examples for the influence of food- and nutrient-sensing on lifespan and stress resilience. On the other hand, studies in highly social insects, such as honey bees, have revealed how social context can shape very plastic life-history traits, for example flexible aging dynamics in the helper caste (workers). It is, however, not understood how food perception and stress resilience are connected in honey bee workers with different social task behaviors and aging dynamics. To explore this linkage, we tested if starvation resilience, which normally declines with age, depends on food responsiveness in honey bees. We studied two typically non-senesced groups of worker bees with different social task behaviors: mature nurses (caregivers) and mature foragers (food collectors). In addition, we included a group of old foragers for which functional senescence is well-established. Bees were individually scored for their food perception by measuring the gustatory response to different sucrose concentrations. Subsequently, individuals were tested for survival under starvation stress. We found that starvation stress resilience, but not gustatory responsiveness differed between workers with different social task behaviors (mature nurses vs. mature foragers). In addition starvation stress resilience differed between foragers with different aging progressions (mature foragers vs. old foragers). Control experiments confirmed that differences in starvation resilience between mature nurses and mature foragers were robust against changing experimental conditions, such as water provision and activity. For all worker groups we established that individuals with low gustatory responsiveness were more resilient to starvation stress. Finally, for the group of rapidly aging foragers we found that low food responsiveness was linked to a delayed age-related decline in starvation resilience. Our study highlights associations between reduced food perception, increased survival capacity and delayed aging in highly social honey bees. We discuss that these associations may involve canonical internal nutrient sensing pathways, which are shared between honey bees and animal models with less plastic aging dynamics.