Long-lived Temnothorax ant queens switch from investment in immunity to antioxidant production with age

Matteo Antoine Negroni,Susanne Foitzik,Barbara Feldmeyer

doi:10.1038/s41598-019-43796-1

Matteo Antoine Negroni, Susanne Foitzik + Show 1 more

Open Access

https://doi.org/10.1038/s41598-019-43796-1

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Abstract

Senescence is manifested by an increase in molecular damage and a deterioration of biological functions with age. In most organisms, body maintenance is traded-off with reproduction. This negative relationship between longevity and fecundity is also evident on the molecular level. Exempt from this negative trait association, social insect queens are both extremely long-lived and highly fecund. Here, we study changes in gene expression with age and fecundity in ant queens to understand the molecular basis of their long lifespan. We analyse tissue-specific gene expression in young founding queens and old 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. Young founding queens invested in immunity (i.e. activation of Toll signalling pathway) and resistance against environmental and physiological stress (i.e. down-regulation of TOR pathway). Conversely, established older queens invested into anti-aging mechanisms through an overproduction of antioxidants (i.e. upregulation of catalase, superoxide dismutase). Finally, we identified candidate genes and pathways, potentially involved in the association between fertility and longevity in social insects and its proximate basis.

Highlights

Senescence occurs in almost all organisms, despite the fact that it increases intrinsic mortality[1]
The hierarchical sample clustering analysis revealed that gene expression differed more strongly between tissue types than between age classes
Clustering by age classes were more pronounced in the fat body than in the brain

Summary

Introduction

Senescence occurs in almost all organisms, despite the fact that it increases intrinsic mortality[1]. The inhibition of those pathways through dietary restriction inhibits cell growth and had a negative effect on fecundity, but improves stress resistance Those observations suggest that in social insects (i) certain pathways or biological processes may be differently regulated compared to Drosophila[19], and/or (ii) that queens receive processed food from workers with a specific composition that modifies the effects of nutrients on lifespan[20,21]. Recent studies focussing on gene expression differences between castes and variation with age point towards a complex link between molecular damage, repair mechanisms and lifespan, which are potentially species-specific, and suggest that investments in fecundity and body maintenance may shift during an ants’ life[5,24,25,26]

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