Evaluating proximate causes of longevity in ant queens by RNA-sequencing

Why organisms age and why some species do so at a faster rate than others are fundamental questions in biology. The queens of perennial eusocial insects (ants, honeybees and termites) are extraordinarily long-lived compared with females of solitary insects. Similar to the reproductive females of eusocial mammals, they do not exhibit signs of functional senescence and terminate reproduction only shortly before they die. In contradiction to the widespread fecundity/longevity trade-off, lifespan and reproductive success seem to be positively associated in eusocial animals. Evolutionary theories explain the long lifespan of queens from their low extrinsic mortality. They live in sheltered, often subterraneous nests, and are cared for by the workers. Furthermore, the queens of eusocial insects use the sperm of only one or a few males to fertilize all their eggs. The lifelong pair bond between males and females predicts that both partners benefit from an increased lifespan of the queen. If and how the reproductive females of eusocial insects avoid the costs of reproduction are open questions. In this study, the myrmicine ant Cardiocondyla obscurior served as a model to investigate the regulation of queen longevity on the proximate level. Due to their relative short life expectancy, the survival and lifetime reproductive success of C. obscurior queens could be monitored in the laboratory. This study is the first to report age-related changes in the transcriptome of mature social insect queens and shows that these changes are exactly opposite to what has previously been reported to aging females of fruit flies, Drosophila melanogaster. The results match the opposing reproductive and mortality patterns observed in social and solitary species and provide a first mechanistic explanation for the simultaneous increase of fecundity and longevity in ant queens (chapter 2). The compensation of putative reproductive costs has not been thoroughly investigated in social insect queens. To test the prediction that reproduction competes for energy and nutrients with other processes, ant queens were forced to increase their investment into somatic repair. This experiment provides clear evidence on the phenotypic and transcriptome level that queens reallocate resources between the reproductive and immune systems (chapter 3). The positive effect of mating on queen longevity was addressed in three analyses (chapter 2, 4 and 5). Physiological changes could be identified which are attributable to mating independent of reproduction (chapter 2) and the male type with whom the queen had mated (chapter 4 and 5). In conclusion, this study suggests an alternative regulation of the conserved pathways that mediate the interplay among reproduction, metabolism and longevity. Queens might not avoid the costs of reproduction, but the costs of self-maintenance which are possibly borne by the workers