Intergenerational transfers may have decoupled physiological and chronological age in a eusocial insect

Abstract

Life-history theory generally predicts that there should be no selection for longevity beyond the limit of reproductive capacity. However, the capacity to increase fitness may not end when individuals reach a state of functional sterility. Recent studies show that intergenerational transfers of resources from post-reproductive parents can increase the offspring's fitness, and analytical theory shows that age-trajectories of transfers may shape the course of senescence in social organisms. In eusocial insects, female roles are partitioned so that one phenotype or "caste" reproduces while another is responsible for resource transfers: the reproductive "queens" are arrested in a continuous reproductive mode, while transfer-activities such as hygienic behaviors, guarding, foraging and further food processing ("nursing") that increases the nutritional value of provisions are conducted by sterile "workers". Worker honey bees normally perform these tasks in a sequence so that nursing inside the protected nest is conducted prior to more risky exterior hive activities such as guarding and foraging. However, foragers may revert to nurse-activity in response to demographic changes, and worker bees can also develop into a stress resistant survival form with a 10-fold increase in lifespan. This elastic division of parental functions is believed to increase colony fitness. Further, it generates a stage-dependent trajectory of senescence that is difficult to address with established theories of aging. In the following, we show how a recent theory that includes resource transfers can be used to elucidate patterns of senescence in eusocial, non-reproducing individuals like the honey bee worker.

Fig. 1

Temporal transfer dynamics in honey bee workers. The black full line is the net transfer of proteinacious jelly by age, and the black dotted line is the net transfer of foraged foods by age. These patterns are typical during the favorable season. The red full line is the net transfer of jelly by a bee that develops into a diutinus worker at the onset of an unfavorable period. The diutinus workers also consume stored honey; thus, the red dotted line depicts this negative net transfer of foraged foods. As conditions improve, the diutinus workers transform into nurse bees and foragers. At this time, they develop the temporal transfer dynamics shown by the black lines.

Fig. 2

Plastic senescence in honey bee workers. A worker can switch between three phenotypes with distinct aging rates. Inter-individual variation in the timing of these shifts generates aging patterns where the physiological and chronological age of the bees are largely decoupled. (A) A worker that receives little or no transfers of jelly during the first days of adult life will bypass the nurse-stage and become a precocious forager. (B) During the favorable season, a worker will normally engage in nurse-activities before it initiates foraging. (C) Foragers in colonies that experience a dramatic loss of young nurse bees can revert to nursing. Diutinus workers initiate foraging (D) and nurse-activities (E) after the unfavorable season.

Fig. 3

Representation of the investment embodied in honey bee workers. Patterns during the favorable and unfavorable season are depicted by full and dash-dotted lines, respectively. The red circle identifies the relative time of onset of foraging. The dotted line exemplifies the investment in a bee that receives little or no proteinacious jelly after emergence. The dynamics match the relative vitellogenin concentrations of the bees accurately (e.g., Engels and Fahrenhorst, 1974; Fluri et al., 1982; Amdam et al., 2004a).