Transcriptomic Signatures Mirror the Lack of the Fecundity/Longevity Trade-Off in Ant Queens

Abstract

Life-history theory predicts a trade-off between reproductive investment and self-maintenance. The negative association between fertility and longevity found throughout multicellular organisms supports this prediction. As an important exception, the reproductives of many eusocial insects (ants, bees, and termites) are simultaneously very long-lived and highly fertile. Here, we examine the proximate basis for this exceptional relationship by comparing whole-body transcriptomes of differently aged queens of the ant Cardiocondyla obscurior. We show that the sets of genes differentially expressed with age significantly overlap with age-related expression changes previously found in female Drosophila melanogaster. We identified several developmental processes, such as the generation of neurons, as common signatures of aging. More generally, however, gene expression in ant queens and flies changes with age mainly in opposite directions. In contrast to flies, reproduction-associated genes were upregulated and genes associated with metabolic processes and muscle contraction were downregulated in old relative to young ant queens. Furthermore, we searched for putative C. obscurior longevity candidates associated with the previously reported lifespan-prolonging effect of mating by comparing the transcriptomes of queens that differed in mating and reproductive status. We found 21 genes, including the putative aging candidate NLaz (an insect homolog of APOD), which were consistently more highly expressed in short-lived, unmated queens than in long-lived, mated queens. Our study provides clear evidence that the alternative regulation of conserved molecular pathways that mediate the interplay among mating, egg laying, and aging underlies the lack of the fecundity/longevity trade-off in ant queens.

Keywords: RNA-Seq; aging; fecundity/longevity trade-off; mating; social insect; transcriptome.

Fig. 1.

Principal component analysis plot of the top 500 genes with highest variance across all samples illustrating variation within and between treatments. Variance stabilizing transformation of expression values was performed prior to analysis. The labels represent the center of mass of each group.

Fig. 2.

Overlap of age- and mating-associated expression patterns. Venn diagrams showing the general overlap between all four comparisons (left) and specifically the overlap of genes upregulated with age in the mated queen type and downregulated in virgin compared with mated or sham-mated queens (top right) as well as vice versa (bottom right).

Fig. 3.

Expression of all 21 mating-associated genes across all four conditions. Illustrated are mean and standard errors of log2-values of normalized counts. Genes are named according to Drosophila melanogaster orthologs/homologs if present and grouped by functions.

Fig. 4.

Relation of expression changes (log2 fold changes = lfc) of genes showing age-regulated transcription in Cardiocondyla obscurior and Drosophila melanogaster. Ten genes were consistently upregulated in aged (Pletcher et al. 2002) and very old flies (Doroszuk et al. 2012) and downregulated in ant queens: ref(2)P, emp, IscU, P5cr-2, CAP, CCHa2, CG3168, CG13124, CG9701, CG11796. For these genes, the mean lfc of both analyses is given.