Dataset Information

Worker-dependent gut symbiosis in an ant.

ABSTRACT: The hallmark of eusocial insects, honeybees, ants, and termites, is division of labor between reproductive and non-reproductive worker castes. In addition, environmental adaption and ecological dominance are also underpinned by symbiotic associations with beneficial microorganisms. Microbial symbionts are generally considered to be maintained in an insect colony in two alternative ways: shared among all colony members or inherited only by a specific caste. Especially in ants, the reproductive caste plays a crucial role in transmission of the symbionts shared among colony members over generations. Here, we report an exceptional case, the worker-dependent microbiota in an ant, Diacamma cf. indicum from Japan. By collecting almost all the individuals from 22 colonies in the field, we revealed that microbiota of workers is characterized by a single dominant bacterium localized at the hindgut. The bacterium belonging to an unclassified member within the phylum Firmicutes, which is scarce or mostly absent in the reproductive castes. Furthermore, we show that the gut symbiont is acquired at the adult stage. Collectively, our findings strongly suggest that the specific symbiont is maintained by only workers, demonstrating a novel pattern of ant-associated bacterial symbiosis, and thus further our understanding of host-microbe interactions in the light of sociobiology.

SUBMITTER: Shimoji H

PROVIDER: S-EPMC9723695 | biostudies-literature | 2021 Oct

REPOSITORIES: biostudies-literature

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Worker-dependent gut symbiosis in an ant.

Shimoji Hiroyuki H Itoh Hideomi H Matsuura Yu Y Yamashita Rio R Hori Tomoyuki T Hojo Masaru K MK Kikuchi Yoshitomo Y

ISME communications 20211028 1

The hallmark of eusocial insects, honeybees, ants, and termites, is division of labor between reproductive and non-reproductive worker castes. In addition, environmental adaption and ecological dominance are also underpinned by symbiotic associations with beneficial microorganisms. Microbial symbionts are generally considered to be maintained in an insect colony in two alternative ways: shared among all colony members or inherited only by a specific caste. Especially in ants, the reproductive ca ...[more]

PMID: 37938661

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Project description:BackgroundEfficient division of reproductive labor is a crucial characteristic of social insects and underlies their ecological and evolutionary success. Despite of the harmonious appearance of insect societies, nestmates may have different interests concerning the partitioning of reproduction among group members. This may lead to conflict about reproductive rights. As yet, few studies have investigated the allocation of reproduction among queens in multi - queen societies ("reproductive skew"). In the ant Leptothorax acervorum, reproductive skew varies considerably among populations. While reproduction is quite equally shared among nestmate queens in most populations from boreal Eurasia (low skew), colonies from populations at the edge of the species' range are characterized by "functional monogyny," i.e., high skew. The proximate mechanisms underlying high skew, in particular how workers influence which queen lays eggs, are not well understood. We investigated the behavior of queens and workers in functionally monogynous colonies of L. acervorum from two mountain ranges in central Spain.ResultsWe provide evidence for both queen and worker influence on the outcome of conflict over reproduction in colonies of L. acervorum from Spain. The patterns of queen - queen aggression and worker - queen grooming and feeding after hibernation allowed predicting, which queen later began to lay eggs. In contrast, worker aggression towards queens was not clearly associated with a queen's future reproductive success. Queen - queen and worker - queen aggression differed in quality: queens typically engaged in ritualized dominance behavior, such as antennal boxing, while workers also attacked queens by biting and prolonged pulling on their legs and antennae. In several cases, overt worker aggression led to the expulsion of queens from the nest or their death.ConclusionWe conclude that queens of L. acervorum from Spain establish rank orders by ritualized dominance interactions, such as antennal boxing. Workers may reinforce these hierarchies by preferentially feeding and grooming high ranking queens and attacking lower ranking queens. Aggressive worker policing may thus stabilize functional monogyny. Optimal skew models predict that high skew in ants is associated with high dispersal costs. In central Spain, L. acervorum is restricted to small patches at higher elevations, which presumably makes dispersal and colony founding difficult. Because of the ecological requirements of L. acervorum and the predicted large impact of global change on central Spain, the functionally monogynous populations of this ant must be considered as threatened.

Dataset Information

Worker-dependent gut symbiosis in an ant.

Publications

Worker-dependent gut symbiosis in an ant.

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