Aging without functional senescence in honey bee workers

Senescence can be defined demographically as an agedependent increase in mortality risk, or functionally as a decline in performance. The relationship between the two phenomena is central for understanding the biological aging process and the implications of human lifespan extension [1]. Generally, demographic and functional senescence are believed to be tightly linked [1], because aging involves a performance decline in multiple body functions, leading to increased mortality. The limited existing data support a direct connection between old age, increased mortality rate and decreased behavioral or physiological performance in organisms ranging from flies [2] to humans [3]. A recent study [4], however, suggests that the linkage may be less universal than previously postulated. To investigate this linkage directly in the non-traditional aging model Apis mellifera [5], old honey bee workers were studied with respect to survival and performance. A test battery of behavioral assays showed a significant increase in experimental mortality rate with chronological age, but no evidence for an age-dependent performance decline in locomotion, learning or responsiveness to light or sucrose. The explanation for this decoupling of intrinsic mortality and functional decline may lie in the social evolution of honey bees [6]. Multiple cohorts of bees between 26 and 52 days old were simultaneously sampled and studied for intrinsic mortality and performance in four diverse behavioral modalities that are central for the workers’ foraging function (detailed experimental procedures are in the Supplemental data available on-line with this issue). Lightresponse scores increased slightly but significantly with age (B = 0.03, R2 = 0.01, F(1,399) = 4.6, p = 0.03; Figure 1A), indicating a weak gain of function instead of the expected loss of functionality during aging. Performance during the light response assay was not different (F(1,344) = 0.84, p = 0.36) between bees dying or surviving during the remainder of the experiment, suggesting that our results cannot be explained by demographic selection. Sucrose responsiveness was unaffected by age (B = 0.001, R2 = 0.00, F(1,293) = 0.002, p = 0.96; Figure 1B); however, light responsiveness and sucrose responsiveness were correlated in bees (R = 0.22, n = 166, p = 0.004), consistent with previous results [7]. Responsiveness to sucrose and light is crucial for the workers’ functioning as foragers and has been linked to a fundamental social behavioral syndrome [8]. Associative learning performance was correlated with the bees’ sucrose responsiveness (R = 0.22, n = 114, p = 0.016), similar to previous studies [9]. Acquisition scores, however, were not influenced by age (B = 0.03, R2 = 0.03, F(1,113) = 3.7, p = 0.06; Figure 1C) and statistical accounting for the bees’ perception of the sucrose reward did not change this conclusion (multiple regression: βsucrose = 0.19, p = 0.055; βage = 0.14, p = 0.146). Presumably, the old workers in this study were invariably foragers with very few exceptions. However, to eliminate the age-dependent division of labor of honey bee workers as a potential explanation of our results, the behavioral analyses were restricted to the older 50% of experimental bees. No relationship between age and any behavioral performance