The sensitivity of a honeybee colony to worker mortality depends on season and resource availability.

Background: Honeybees have extraordinary phenotypic plasticity in their senescence rate, making them a fascinating model system for the evolution of aging. Seasonal variation in senescence and extrinsic mortality results in a tenfold increase in worker life expectancy in winter as compared to summer. To understand the evolution of this remarkable pattern of aging, we must understand how individual longevity scales up to effects on the entire colony. In addition, threats to the health of honey bees and other social insects are typically measured at the individual level. To predict the effects of environmental change on social insect populations, we must understand how individual effects impact colony performance. We develop a matrix model of colony demographics to ask how worker age-dependent and age-independent mortality affect colony fitness and how these effects differ by seasonal conditions.

Results: We find that there are seasonal differences in honeybee colony elasticity to both senescent and extrinsic worker mortality. Colonies are most elastic to extrinsic (age-independent) nurse and forager mortality during periods of higher extrinsic mortality and resource availability but most elastic to age-dependent mortality during periods of lower extrinsic mortality and lower resource availability.

Conclusions: These results suggest that seasonal changes in the strength of selection on worker senescence partly explain the observed pattern of seasonal differences in worker aging in honey bees. More broadly, these results extend our understanding of the role of extrinsic mortality in the evolution of senescence to social animals and improve our ability to model the effects of environmental change on social insect populations of economic or conservation concern.