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

ABSTRACT: 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.

ORGANISM(S): Temnothorax rugatulus

PROVIDER: GSE111415 | GEO | 2018/03/06

REPOSITORIES: GEO

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Project description:In many animals living in groups the reproductivestatus of individuals is determined by their social status. In specieswith social hierarchies, the death of dominant individuals typicallyupheaves the social hierarchy and provides an opportunity for subordinateindividuals to improve their social status. Such a phenomenon occursin the monogyne form of the fire ant\emph{, Solenopsis invicta, }wherecolonies typically contain a single wingless reproductive queen, thousandsof workers and hundreds of winged non-reproductive virgin queens.Upon the death of the mother queen, many virgin queens shed theirwings and initiate reproductive development instead of departing ona mating flight. Workers progressively execute almost all of themover the following weeks. The workers base their collective decisionon pheromonal cues associated with the onset of reproductive developmentof the virgin queens which occurs after orphaning. To examine the factors that determine which virgin queens are executed and which survive, we set up artificial competitions between queens from different colonies. Using microarrays, we found that queens from winning colonies showed higher mitochondrial as well as organ development activities 24 hours after orphaning than did queens from colonies that lost the competitions. Furthermore, queens from colonies where queens shed their wings faster after orphaning were more likely to survive competitions. Finally, higher wing shedding speed is linked to higher mitochondrial activity. Eight competitions were initially conducted between queens form pairs of colonies. Six competitions clearly identified one winning colony and one losing colony. We thus have microarray data for six competitions (ie biological replicates), with one winning and one losing colony within each competition. Thus 12 colonies total. For each colony, RNA extracted from five queens was pooled, and hybridized against an unrelated common reference RNA that had been made from a pool of many S. invicta individuals of all castes and developmental stages. Lab work was conducted in blocks (by competition) with randomized order within competition to avoid introducing bias. No technical replication was performed.

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

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