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The early life of a leaf-cutter ant colony constrains symbiont vertical transmission and favors horizontal transmission.

ABSTRACT: Colonial organisms host a large diversity of symbionts (collectively, parasites, mutualists, and commensals) that use vertical transmission (from parent colony to offspring colony) and/or horizontal transmission to disperse between host colonies. The early life of some colonies, characterized by the dispersal and establishment of solitary individuals, may constrain vertical transmission and favor horizontal transmission between large established colonies. We explore this possibility with the miniature cockroach Attaphila fungicola, a symbiont of leaf-cutter ants and the mutualist fungal gardens they cultivate. The early life of a leaf-cutter colony is characterized by the dispersal of a female alate (winged "queen") carrying a fungal pellet, and the subsequent establishment of a foundress (workerless "queen") raising her incipient fungal garden and colony. Roaches hitchhike on female alates during leaf-cutter nuptial flights, which strongly suggests that roaches are vertically transmitted to foundresses and their incipient colonies; however, weak compatibility between roaches and incipient gardens may constrain roach vertical transmission. Reciprocally, opportunities for horizontal transmission between large established colonies with abundant fungal gardens may weaken selection against roach-induced harm (virulence) of incipient gardens. We use a laboratory experiment, behavioral observations, field surveys, and a transmission model to estimate the effect roaches have on the survivorship of incipient gardens and the frequency of roach vertical transmission. Contrary to traditional assumptions, our results indicate that roaches harm incipient gardens and predominantly use horizontal transmission between established leaf-cutter colonies. Ultimately, "costs of generalism" associated with infecting disparate stages of a host's lifecycle (e.g., incipient vs. established colonies) may constrain the vertical transmission of roaches and a broad range of symbionts.

SUBMITTER: Phillips ZI

PROVIDER: S-EPMC8427574 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundLeaf-cutter ants use fresh plant material to grow a mutualistic fungus that serves as the ants' primary food source. Within fungus gardens, various plant compounds are metabolized and transformed into nutrients suitable for ant consumption. This symbiotic association produces a large amount of refuse consisting primarily of partly degraded plant material. A leaf-cutter ant colony is thus divided into two spatially and chemically distinct environments that together represent a plant biomass degradation gradient. Little is known about the microbial community structure in gardens and dumps or variation between lab and field colonies.Methodology/principal findingsUsing microbial membrane lipid analysis and a variety of community metrics, we assessed and compared the microbiota of fungus gardens and refuse dumps from both laboratory-maintained and field-collected colonies. We found that gardens contained a diverse and consistent community of microbes, dominated by Gram-negative bacteria, particularly gamma-Proteobacteria and Bacteroidetes. These findings were consistent across lab and field gardens, as well as host ant taxa. In contrast, dumps were enriched for Gram-positive and anaerobic bacteria. Broad-scale clustering analyses revealed that community relatedness between samples reflected system component (gardens/dumps) rather than colony source (lab/field). At finer scales samples clustered according to colony source.Conclusions/significanceHere we report the first comparative analysis of the microbiota from leaf-cutter ant colonies. Our work reveals the presence of two distinct communities: one in the fungus garden and the other in the refuse dump. Though we find some effect of colony source on community structure, our data indicate the presence of consistently associated microbes within gardens and dumps. Substrate composition and system component appear to be the most important factor in structuring the microbial communities. These results thus suggest that resident communities are shaped by the plant degradation gradient created by ant behavior, specifically their fungiculture and waste management.

Project description:Many fungus-growing ants engage in a defensive symbiosis with antibiotic-producing ectosymbiotic bacteria in the genus Pseudonocardia, which help protect the ants' fungal mutualist from a specialized mycoparasite, Escovopsis. Here, using germfree ant rearing and experimental pathogen infection treatments, we evaluate if Acromyrmex ants derive higher immunity to the entomopathogenic fungus Metarhizium anisopliae from their Pseudonocardia symbionts. We further examine the ecological dynamics and defensive capacities of Pseudonocardia against M. anisopliae across seven different Acromyrmex species by controlling Pseudonocardia acquisition using ant-nonnative Pseudonocardia switches, in vitro challenges, and in situ mass spectrometry imaging (MSI). We show that Pseudonocardia protects the ants against M. anisopliae across different Acromyrmex species and appears to afford higher protection than metapleural gland (MG) secretions. Although Acromyrmex echinatior ants with nonnative Pseudonocardia symbionts receive protection from M. anisopliae regardless of the strain acquired compared with Pseudonocardia-free conditions, we find significant variation in the degree of protection conferred by different Pseudonocardia strains. Additionally, when ants were reared in Pseudonocardia-free conditions, some species exhibit more susceptibility to M. anisopliae than others, indicating that some ant species depend more on defensive symbionts than others. In vitro challenge experiments indicate that Pseudonocardia reduces Metarhizium conidiospore germination area. Our chemometric analysis using matrix-assisted laser desorption/ionization mass spectrometry imaging (MALDI-MSI) reveals that Pseudonocardia-carrying ants produce more chemical signals than Pseudonocardia-free treatments, indicating that Pseudonocardia produces bioactive metabolites on the Acromyrmex cuticle. Our results indicate that Pseudonocardia can serve as a dual-purpose defensive symbiont, conferring increased immunity for both the obligate fungal mutualist and the ants themselves. IMPORTANCE In some plants and animals, beneficial microbes mediate host immune response against pathogens, including by serving as defensive symbionts that produce antimicrobial compounds. Defensive symbionts are known in several insects, including some leaf-cutter ants where antifungal-producing Actinobacteria help protect the fungal mutualist of the ants from specialized mycoparasites. In many defensive symbioses, the extent and specificity of defensive benefits received by the host are poorly understood. Here, using "aposymbiotic" rearing, symbiont switching experiments, and imaging mass spectrometry, we explore the ecological and chemical dynamics of the model defensive symbiosis between Acromyrmex ants and their defensive symbiotic bacterium Pseudonocardia. We show that the defensive symbiont not only protects the fungal crop of Acromyrmex but also provides protection from fungal pathogens that infect the ant workers themselves. Furthermore, we reveal that the increased immunity to pathogen infection differs among strains of defensive symbionts and that the degree of reliance on a defensive symbiont for protection varies across congeneric ant species. Taken together, our results suggest that Acromyrmex-associated Pseudonocardia have evolved broad antimicrobial defenses that promote strong immunity to diverse fungal pathogens within the ancient fungus-growing ant-microbe symbiosis.

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The early life of a leaf-cutter ant colony constrains symbiont vertical transmission and favors horizontal transmission.

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