Shift in worker physiology and gene expression pattern from reproductive to diapause-like with colony age in the bumble bee Bombus impatiens

Insects maximize their fitness by exhibiting predictable and adaptive seasonal patterns in response to changing environmental conditions. These seasonal patterns are often expressed even when insects are kept in captivity, suggesting they are functionally and evolutionarily important. In this study, we examined whether workers of the eusocial bumble bee Bombus impatiens maintained a seasonal signature when kept in captivity. We used an integrative approach and compared worker egg laying, ovarian activation, body size and mass, lipid content in the fat body, cold tolerance and expression of genes related to cold tolerance, metabolism and stress throughout colony development. We found that bumble bee worker physiology and gene expression patterns shift from reproductive-like to diapause-like as the colony ages. Workers eclosing early in the colony cycle had increased egg laying and ovarian activation, and reduced cold tolerance, body size, mass and lipid content in the fat body, in line with a reproductive-like profile, while late-eclosing workers exhibited the opposite characteristics. Furthermore, expression patterns of genes associated with reproduction and diapause differed between early- and late-eclosing workers, partially following the physiological patterns. We suggest that a seasonal signature, innate to individual workers, the queen or the colony, is used by workers as a social cue determining the phenology of the colony and discuss possible implications for understanding reproductive division of labor in bumble bee colonies and the evolutionary divergence of female castes in the genus Bombus.