How can ant queens live so long? Genes of multiple longevity pathways change expression with age in the ant Temnothorax rugatulus

Senescence is manifested by an increase in oxidative stress and a decline in biological functions with age. In most organisms, body maintenance is traded-off with reproduction. The negative relationship between longevity and fecundity is also evident on the molecular level, yet the proximate mechanisms remain poorly understood. Apparently by-passing this trade-off, social insect queens are both extremely long-lived (up to 30 years in some ants) and highly fecund compared to workers. Here, we study changes in gene expression with age and fecundity in queens to determine how the trade-off between those two traits is reshaped. We analyse tissue-specific gene expression in young founding queens and old, highly fecund queens of the ant Temnothorax rugatulus. More genes altered their expression with age in the fat body than in the brain. Despite strong differences in ovary development, few fecundity genes were differentially expressed. However, many longevity genes involved in well-known pathways or lifespan-associated biological processes changed their expression with age indicating that multiple longevity mechanisms are activated successively throughout a queens’ life. Young queens invested in immunity (i.e. activation of the Toll signalling pathway) and resistance against environmental and physiological stress associated with the founding phase (i.e. down regulation of the TOR pathway), while established older queens up-regulate anti-aging mechanisms (i.e. up-regulation of catalase, superoxide dismutase, heat shock 70 kDa proteins). Finally, we identified a number of candidate genes and pathways, potentially involved in reshaping the fertility-longevity trade-off in social insects, shedding light on how this is achieved on a proximate level.