Queen loss increases worker survival in leaf-cutting ants under paraquat-induced oxidative stress

Abstract

Longevity is traded off with fecundity in most solitary species, but the two traits are positively linked in social insects. In ants, the most fecund individuals (queens and kings) live longer than the non-reproductive individuals, the workers. In many species, workers may become fertile following queen loss, and recent evidence suggests that worker fecundity extends worker lifespan. We postulated that this effect is in part owing to improved resilience to oxidative stress, and tested this hypothesis in three Myrmicine ants: Temnothorax rugatulus, and the leaf-cutting ants Atta colombica and Acromyrmex echinatior . We removed the queen from colonies to induce worker reproduction and subjected workers to oxidative stress. Oxidative stress drastically reduced survival, but this effect was less pronounced in leaf-cutting ant workers from queenless nests. We also found that, irrespective of oxidative stress, outside workers died earlier than inside workers did, likely because they were older. Since At. colombica workers cannot produce fertile offspring, our results indicate that direct reproduction is not necessary to extend the lives of queenless workers. Our findings suggest that workers are less resilient to oxidative stress in the presence of the queen, and raise questions on the proximate and ultimate mechanisms underlying socially mediated variation in worker lifespan. This article is part of the theme issue ‘Ageing and sociality: why, when and how does sociality change ageing patterns?’

Ageing and sociality: why, when and how does sociality change ageing patterns?

“…Several studies have shown that reproductives live longer than non-reproductives even when they do not differ in ontogeny and morphology, e.g. as in certain species of ants [34,56,57] and reproducing workers of honeybees [58] and ants [37,40,43]. Similarly, highly fecund queens of Cardiocondyla ants live longer than queens that lay only a few eggs per week [59].…”

“…Majoe et al [37] report that increasing oxidative stress through treatment with paraquat increases the mortality of workers in three ant species. In two of them, this effect is less pronounced in queenless colonies, in which worker reproduction is generally induced, than queenright colonies, where workers typically do not lay eggs.…”

Oxidative stress and senescence in social insects: a significant but inconsistent link?

“…Here our focus is on social insects, among which experimentally induced ROS increase senescence of social bees and ants [6][7][8][9]. One effect of ROS is the oxidation of amino acids in proteins by introducing carbonyl groups, which often leads to a loss of catalytic activity and simultaneously marks the protein for proteolytic degradation (reviewed in [10] and [11]).…”

Reproductive Potential Impacts Body Maintenance Parameters and Global DNA Methylation in Honeybee Workers (Apis mellifera L.)

“…Past research indicated that the longevity of workers decreased with prolonged queenlessness in the field experiment [29]. On the other hand, queenlessness expanded the worker longevity and reproductivity of bees [5,9,10] and ants [30], but only when the queens were absent at the worker larval stage. Hence, the presence of a queen affects longevity of workers in different ways depending on whether the queen is present at their larval or imago stage.…”