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Abstract
Eusocial insects provide special insights into the genetic pathways influencing aging because of their long-lived queens and flexible aging schedules. Using qRT-PCR in the primitively eusocial bumble bee Bombus terrestris (Linnaeus), we investigated expression levels of four candidate genes associated with taxonomically widespread age-related pathways (coenzyme Q biosynthesis protein 7, COQ7; DNA methyltransferase 3, Dnmt3; foraging, for; and vitellogenin, vg). In Experiment 1, we tested how expression changes with queen relative age and productivity. We found a significant age-related increase in COQ7 expression in queen ovary. In brain, all four genes showed higher expression with increasing female (queen plus worker) production, with this relationship strengthening as queen age increased, suggesting a link with the positive association of fecundity and longevity found in eusocial insect queens. In Experiment 2, we tested effects of relative age and social environment (worker removal) in foundress queens and effects of age and reproductive status in workers. In this experiment, workerless queens showed significantly higher for expression in brain, as predicted if downregulation of for is associated with the cessation of foraging by foundress queens following worker emergence. Workers showed a significant age-related increase in Dnmt3 expression in fat body, suggesting a novel association between aging and methylation in B. terrestris. Ovary activation was associated with significantly higher vg expression in fat body and, in younger workers, in brain, consistent with vitellogenin's ancestral role in regulating egg production. Overall, our findings reveal a mixture of novel and conserved features in age-related genetic pathways under primitive eusociality.
Highlights
The occurrence of aging in organisms raises important questions at both evolutionary and mechanistic levels (Hughes and Reynolds, 2005; Parker, 2010; Flatt et al, 2013; Gems and Partridge, 2013)
We investigated gene expression as a function of age, social environment and reproductive status for a set of candidate genes associated with taxonomically widespread age-related genetic pathways in queens and workers of the bumble bee Bombus terrestris (Linnaeus)
In Experiment 1, for coenzyme Q biosynthesis protein 7 (COQ7) in brain, queens showed significantly higher expression with decreasing male production (LR = 4.40, d.f. = 1, P = 0.036; Table S3). This association was absent for COQ7 expression in ovary and there was no significant relationship between gene expression and male production for DNA methyltransferase 3 (Dnmt3) and for in either brain or ovary or for vg in ovary (Table S3)
Summary
The occurrence of aging in organisms raises important questions at both evolutionary and mechanistic levels (Hughes and Reynolds, 2005; Parker, 2010; Flatt et al, 2013; Gems and Partridge, 2013). In eusocial insects, aging can be regulated by the social environment and even reversed within the lifespan of individuals (Huang and Robinson, 1996; Amdam et al, 2005; Smedal et al, 2009; Amdam, 2011; Woodard et al, 2013). All these traits point, in eusocial insects, to a large degree of flexibility and responsiveness in the genetic pathways that influence aging
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