Worker-dependent gut symbiosis in an ant

Hiroyuki Shimoji,Hideomi Itoh,Rio Yamashita,Masaru K Hojo,Yu Matsuura,Tomoyuki Hori,Yoshitomo Kikuchi

doi:10.1038/s43705-021-00061-9

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.

Highlights

Symbiotic bacteria affect the fitness of the host animals by altering the life cycle, reproductive system, nutritional status, and physiological/behavioral traits in a wide range of taxa [1,2,3]
As an example of phenotypic change caused by symbiotic bacteria, Russell et al [ref. 13] suggest that gut symbionts have mediated the evolution of herbivory in ants by supplying nutrients
operational taxonomic unit (OTU)-based analysis showed that microbiota of 99/105 foragers samples (94%), 6/22 gamergate samples (27%) were occupied by one extreme dominant OTU (OTU01; ≥ 50% relative abundance; Fig. 2d, e), belonging to unclassified member of the phylum Firmicutes

Summary

Introduction

Symbiotic bacteria affect the fitness of the host animals by altering the life cycle, reproductive system, nutritional status, and physiological/behavioral traits in a wide range of taxa [1,2,3]. Extensive studies have shown remarkable diversity of symbiotic relationships between insects and bacteria, in which novel biological functions, transmission modes, and coevolutionary processes of the symbioses have been unraveled [4]. Obligate symbiosis, such as the aphid-Buchnera symbiosis, is one of the spectacular events of the major evolutionary transitions from eukaryotic cells to more complex organisms [5]. The ecological success of ants has been achieved by the evolution of sophisticated eusociality, and underpinned by symbiotic relationships with other associated organisms [7,8,9]. Bacterial symbiosis underlies ecological success of ant societies in various manners

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Conclusion