Queens of the inquiline social parasite Acromyrmex insinuator can join nest-founding queens of its host, the leaf-cutting ant Acromyrmex echinatior

Queens of the inquiline social parasite Acromyrmex insinuator are known to infiltrate mature colonies of Acromyrmex echinatior and to exploit the host’s perennial workforce by producing predominantly reproductive individuals while suppressing host reproduction. Here we report three cases of an A. insinuator queen having joined an incipient colony of A. echinatior that contained only the founding host-queen and her small symbiotic fungus garden. We conjectured that 1:1 host-inquiline co-founding—a phenomenon that has only rarely been reported in ants—may imply that the presence of an A. insinuator queen may incur benefits to the host by increasing survival of its incipient colonies. We observed that the parasite queens neither foraged nor defended the nest against intruders. However, the parasite queens interacted with the host and fungus in a way that could be consistent with grooming and/or with contributing eggs. These observations may help explain why A. insinuator queens have maintained metapleural glands, even though they are smaller than those of host queens, and why A. insinuator has lost the large foraging worker caste but not the small worker caste.

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

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?’

Biomineral armor in leaf-cutter ants

Although calcareous anatomical structures have evolved in diverse animal groups, such structures have been unknown in insects. Here, we report the discovery of high-magnesium calcite [CaMg(CO3)2] armor overlaying the exoskeletons of major workers of the leaf-cutter ant Acromyrmex echinatior. Live-rearing and in vitro synthesis experiments indicate that the biomineral layer accumulates rapidly as ant workers mature, that the layer is continuously distributed, covering nearly the entire integument, and that the ant epicuticle catalyzes biomineral nucleation and growth. In situ nanoindentation demonstrates that the biomineral layer significantly hardens the exoskeleton. Increased survival of ant workers with biomineralized exoskeletons during aggressive encounters with other ants and reduced infection by entomopathogenic fungi demonstrate the protective role of the biomineral layer. The discovery of biogenic high-magnesium calcite in the relatively well-studied leaf-cutting ants suggests that calcareous biominerals enriched in magnesium may be more common in metazoans than previously recognized.

Biomineral armor in leaf-cutter ants

Although calcareous anatomical structures have evolved in diverse animal groups, such structures have been unknown in insects. Here, we report the discovery of high-magnesium calcite [CaMg(CO3)2] armor overlaying the exoskeletons of major workers of the leaf-cutter ant Acromyrmex echinatior. Live-rearing and in vitro synthesis experiments indicate that the biomineral layer accumulates rapidly as ant workers mature, that the layer is continuously distributed, covering nearly the entire integument, and that the ant epicuticle catalyzes biomineral nucleation and growth. In situ nanoindentation demonstrates that the biomineral layer significantly hardens the exoskeleton. Increased survival of ant workers with biomineralized exoskeletons during aggressive encounters with other ants and reduced infection by entomopathogenic fungi demonstrate the protective role of the biomineral layer. The discovery of biosynthesized high-magnesium calcite in the relatively well-studied leaf-cutting ants suggests that calcareous biominerals enriched in magnesium may be more common in metazoans than previously recognized.

Fungus-Growing Ant's Microbial Interaction of Streptomyces sp. and Escovopsis sp. through Molecular Networking and MALDI Imaging

Microbes associated with fungus-growing ants represent a poorly explored source of natural products. In this study, we used mass spectrometry-based dereplication techniques for identifying a set of secondary metabolites produced during the microbial interaction between Streptomyces sp. (CB0028) and Escovopsis sp. (CBAcro424). Both microorganisms were isolated from the nest of the fungus-growing ant Acromyrmex echinatior. Through MALDI imaging and MS/MS molecular networking, we annotated the siderophores: desferrioxamine B (1), ferrioxamine B (2), ferrioxamine E (3) and the N-formylated peptide SCO-2138/SLI-2138 (4). MALDI imaging experiments suggest that siderophores occurred during the microbial interactions in the fungus-growing ants – microbes symbioses. This is the first report on the production of compounds 1-4 by bacteria associated with fungus-growing ants.

Queen reproductive tract secretions enhance sperm motility in ants

Queens of Acromyrmex leaf-cutting ants store sperm of multiple males after a single mating flight, and never remate even though they may live for decades and lay tens of thousands of eggs. Sperm of different males are initially transferred to the bursa copulatrix and compete for access to the long-term storage organ of queens, but the factors determining storage success or failure have never been studied. We used in vitro experiments to show that reproductive tract secretions of Acromyrmex echinatior queens increase sperm swimming performance by at least 50% without discriminating between sperm of brothers and unrelated males. Indiscriminate female-induced sperm chemokinesis makes the likelihood of storage directly dependent on initial sperm viability and thus provides a simple mechanism to secure maximal possible reproductive success of queens, provided that initial sperm motility is an accurate predictor of viability during later egg fertilization.