Senescence may evolve in response to externally imposed schedules of survival and reproduction. It may result from cumulative damage to several tissues and organs leading to the progressive malfunction of somatic defences including the immune system, which is a relevant and accessible trait to study the evolution and the mechanisms of senescence. In social insects, reproduction of workers is negligible and their fitness relies on the colony reproductive success, which depends on workers' longevity. Consequently, evolution of senescence in workers will rely on age-dependent survival rate and the residual reproductive value of the colony. Using the bumblebee, Bombus terrestris, as model system, we investigated changes in constitutive and inducible immune defences. Such changes were monitored in relation to worker age and colony age and as well under a high, persistent level of parasitism. The results show that the inducible production of antibacterial peptides was not affected by the age of individual worker or the age of their colony. In contrast, constitutive defences such as haemocyte density and phenoloxidase (PO) activity decline with individual worker age and potential accumulation of physiological defects due to high and persistent levels of parasitism did not explain this pattern of immunosenescence. Interestingly, levels of worker constitutive defences were found to increase with colony age. We found antibacterial activity was strongly traded-off against PO activity. Such a relationship was not caused by resource shortage. Overall, these data suggest that patterns of variation of immune defences with worker age and colony age are likely the result of plastic temporal adjustments of immune responses in accordance with life history predictions. Hence, control of pathogenic threat in a social system may involve optimal adjustments of immune defences at both the individual and colony levels.