Experimental modulation of external microbiome affects nestmate recognition in harvester ants (<i>Pogonomyrmex barbatus</i>)

Abstract. Microbial life is ubiquitous, yet we are just beginning to understand how microbial communities are assembled. We test whether relationships between ant microbiomes and their environments resemble patterns identified in the human home microbiome. We examine the microbial communities and chemical composition of ants, their waste, their nest, and the surrounding soil. We predicted that the microbiome of the canopy ant, Azteca trigona, like that of humans, represents a distinct, relatively invariant, community compared to the soil community. Because Azteca build aboveground nests constructed from ant exudates mixed with chewed plant fibers, we predicted that nest-associated microorganisms should reflect their ants, not the surrounding environment. The ant microbiome was distinct from the soil, but contrary to initial predictions, ant microbiomes varied dramatically across colonies. This variation was largely driven by the relative abundance of Lactobacillus, a genus frequently associated with hymenopteran diets. Despite the origin of nests and their means of construction, nest-associated microorganisms were most similar to the surrounding soil. The microbiota of Azteca ants is thus distinct, but dimorphic across colonies, for reasons likely due to inter-colony differences in diet; microbiotas of the nests however mirror the surrounding soil community, similar to patterns of human home microbiota.

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“…, Dosmann et al. ) or provide protection through production of antimicrobial compounds (Promnuan et al. , Sen et al.…”

Section: Introductionmentioning

confidence: 99%

The microbiome of the ant‐built home: the microbial communities of a tropical arboreal ant and its nest

et al. 2017

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“…In fact, colony identity is conveyed by a highly diverse set of CHCs, and intraspecific and interspecific invaders from other colonies are detected and defended against as a consequence of having a different CHC blend than the blend associated with a particular nest/colony (4). In addition, other non-CHC olfactory stimuli play important roles in ant chemical ecology as alarm, trail, or recognition pheromones and are often found in ant exocrine glands (5) and in the microbiota of the ant cuticle (6).…”

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confidence: 99%

Functional characterization of odorant receptors in the ponerine ant, Harpegnathos saltator

Slone

Pask

Ferguson

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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Animals use a variety of sensory modalities-including visual, acoustic, and chemical-to sense their environment and interact with both conspecifics and other species. Such communication is especially critical in eusocial insects such as honey bees and ants, where cooperation is critical for survival and reproductive success. Various classes of chemoreceptors have been hypothesized to play essential roles in the origin and evolution of eusociality in ants, through their functional roles in pheromone detection that characterizes reproductive status and colony membership. To better understand the molecular mechanisms by which chemoreceptors regulate social behaviors, we investigated the roles of a critical class of chemoreceptors, the odorant receptors (ORs), from the ponerine ant Harpegnathos saltator in detecting cuticular hydrocarbon pheromones. In light of the massive OR expansion in ants (∼400 genes per species), a representative survey based on phylogenetic and transcriptomic criteria was carried out across discrete odorant receptor subfamilies. Responses to several classes of semiochemicals are described, including cuticular hydrocarbons and mandibular gland components that act as H. saltator pheromones, and a range of more traditional general odorants. When viewed through the prism of caste-specific OR enrichment and distinctive OR subfamily odorant response profiles, our findings suggest that whereas individual HsOrs appear to be narrowly tuned, there is no apparent segregation of tuning responses within any discrete HsOr subfamily. Instead, the HsOR gene family as a whole responds to a broad array of compounds, including both cuticular hydrocarbons and general odorants that are likely to mediate distinct behaviors.ant | odorant receptor | odor coding | pheromone T he detection of ecologically relevant chemosensory information is critical to the survival and propagation of all organisms. For example, sex pheromones allow members of the same species to locate and assess mates, and predators use volatile kairomones to locate prey. There is long-standing interest in understanding the pheromonal communication of insects and, in particular, exploring how semiochemicals govern the interactions of eusocial colonies. Ants are intriguing for the purposes of chemosensory studies, because of their diversity and exploitation of cuticular hydrocarbons (CHCs) for nest-mate recognition, and as signals of reproductive and caste status. Most ants live in closed societies within a shared colony or nest-with stereotypic social behaviors that involve a strict division of reproductive labor-in which multiple overlapping generations of sterile workers cooperate to nurture the progeny produced by the reproductives, which usually consist of single or small numbers of long-lived, highly fertile queens and short-lived male drones (1). Reproductive status within the colony is thought to be signaled primarily by a subset of the hydrocarbons secreted onto the external cuticle of insects and other arthropods (e.g. ref.2) that also func...

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“…Such effects may result from the direct actions of the antibiotic or from indirect effects, such as changes in host metabolism or production of nutrients sustaining cuticular bacterial growth. In Drosophila , cuticular microbes have been hypothesized to affect chemical profiles by using CHC as a carbon source or a substrate for degradative enzymes (12), and previous research on Pogonomyrmex ants showed that topical antibiotic administration can alter CHC profiles, confirming a possible role of surface microbes in CHC profile determination (18). However, the same kind of antibiotic treatment applied on Acromyrmex subterraneus did not affect CHC profiles (19).…”

Section: Discussionmentioning

confidence: 97%

“…In Pogonomyrmex barbatus harvester ants, individuals with experimentally-augmented cuticular microbiomes are rejected by nestmates more than controls, whereas antibiotic-treated individuals are not. This suggests that cuticle-dwelling microbes influence nestmate recognition dynamics (18). Contrarily, however, topical antibiotic administration on Acromyrmex subterraneus leafcutter ants does not affect cuticular hydrocarbon profiles (19).…”

Section: Introductionmentioning

confidence: 99%

“…Despites providing insights into the role of symbiotic microbes in CHC-mediated nestmate recognition, these studies either investigate microbial effects through behavioural tests, without correlating CHC measures (17,21), or compare CHC profiles between antibiotic-treated and control individuals without behavioural tests (18–20). To gain more insights into the interplay between gut microbiota and chemical-based social interactions, we here seek to implement an integrative analysis of CHC, gut bacterial communities and nestmate recognition behaviour.…”

Section: Introductionmentioning

confidence: 99%

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The scent of symbiosis: gut bacteria affect social interactions in leafcutting ants

Teseo

Zweden

Pontieri³

et al. 2018

Preprint

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Animal gut microbiota affect host physiology and behaviour. In eusocial Hymenoptera, where colony-level integrity is preserved via a nestmate discrimination system based on cuticular hydrocarbon mixtures, microorganismal effects may influence social dynamics. Although nestmate recognition has undergone a thorough exploration during the last four decades, few studies have investigated the putative role of gut microbes. Here we integrate metagenomic, chemical and behavioural approaches to test whether gut microbes affect nestmate recognition in Acromyrmex echinatior leaf-cutting ants. Treating workers with a sterile diet or with antibiotics resulted in a substantial alteration of their gut microbial communities. In pairwise social interactions, untreated vs. antibiotic-treated nestmates behaved more aggressively than other nestmate and non-nestmate pairs, suggesting that the suppression of microbes indirectly alters chemical social cues and triggers aggressive behaviour. Chemical analyses on treated individuals revealed a decrease in the abundance of two metapleural gland antifungal compounds, and we confirmed the correspondence between aggression levels and chemical profile differences. Feeding microbiota-remodelled ants with conspecific faecal droplets partially restored the original bacterial communities. Furthermore, non-nestmates fed with faecal droplets from different colonies were unusually aggressive compared to pairs fed with faecal droplets from the same colony. This suggests that chemicals derived from microbial strains may shape nestmate recognition, opening novel questions about the role of microorganisms in the evolution of social behaviour.

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Experimental modulation of external microbiome affects nestmate recognition in harvester ants (Pogonomyrmex barbatus)

Cited by 24 publications

References 25 publications

The microbiome of the ant‐built home: the microbial communities of a tropical arboreal ant and its nest

The microbiome of the ant‐built home: the microbial communities of a tropical arboreal ant and its nest

Functional characterization of odorant receptors in the ponerine ant, Harpegnathos saltator

The scent of symbiosis: gut bacteria affect social interactions in leafcutting ants

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