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.

Reproductive protein protects functionally sterile honey bee workers from oxidative stress

“…64). Thus, the bee would exemplify (63) that, by social evolution (46,47,65), reproductive control circuits can be remodeled to extend life. However, this proposition rests on the assumption that the solitary ancestor of the honey bee was characterized by an antagonistic relationship between vitellogenin activity and longevity.…”

Order, Disorder, Death: Lessons from a Superorganism

“…It is widely domesticated as a source of honey and beeswax and a well-known research system for understanding the characteristic differentiation of eusocial individuals into reproductive and sterile forms (Amdam et al, 2004a;Bloch et al, 2002;Robinson et al, 2005). The bee is an established model in systems theory (Mitchell, 2003;Page and Erber, 2002), behavioral ecology (Seeley, 1995), neurobiology (Farooqui et al, 2004;Humphries et al, 2003;Menzel, 1979;Scheiner et al, 2001), and aging (Amdam and Page, 2005;Omholt and Amdam, 2004;Seehuus et al, 2006). It has a rising position in molecular research that is fueled by an emerging availability of functional genomic tools Beye et al, 2002;Omholt et al, 1995;Yu et al, 1997) and a newly annotated genome sequence (www.hgsc.bcm.tmc.edu).…”

“…The adult workers differentiate into three temporal forms referred to as the "nurse bee," the "forager," and the "diutinus worker" stages, respectively (Amdam and Page, 2005). The nurse bee (Fig.…”

“…3) develop during unfavorable periods without opportunities for brood rearing (Amdam and Page, 2005;Maurizio, 1950;Omholt and Amdam, 2004). They differentiate from nurse bees that no longer take care of brood (Amdam and Omholt, 2002;Huang and Robinson, 1995;Omholt and Amdam, 2004).…”

Cellular senescence in honey bee brain is largely independent of chronological age

“…Recently, this eusocial insect caste has also started to contribute to our understanding of aging regulation (Omholt and Amdam, 2004;Amdam and Page, 2005;Amdam et al, 2005a). Worker bees display a flexible pattern of longevity that is interlinked with the alloparental tasks they perform (Amdam and Page, 2005). Typically, a worker engages in nest activities (such as nursing larvae), before she switches to more risky exterior hive activities like guarding and foraging as a 18-28-day-old (Winston, 1987).…”