Within‐colony transmission and the cost of a mutualistic bacterium in the leaf‐cutting ant Acromyrmex octospinosus

Abstract

Summary1. Stable mutualistic interactions require the long-term alignment of fitness interests of participating species. This condition is fulfilled when the benefits of the relationship exceed the costs for all partners. 2. One apparent stabilizing factor in mutualisms is the vertical (parent to offspring) transmission of symbionts, as this tends to reduce the expression of virulent traits and reproductive conflicts. This study examines the cost and mode of transmission of a mutualistic Streptomyces bacterium that grows on the cuticle of leaf-cutting ants and produces antibiotics against a specialized fungal parasite of the ant fungus gardens. 3. It is shown that ant respiration rates are elevated by 10-20% when the bacterium is present on their cuticle. This increase is due to direct respiration of the bacterium and possible excess respiration by the ants. Although these two factors cannot be separated, it is clear that the total increase gives a reasonable quantification of the metabolic costs incurred by the Streptomyces symbiont. 4. Ants that actively maintain Streptomyces cultures on their cuticle tend to consume more of their mutualistic fungus garden than controls and this excess consumption increases with the amount of Streptomyces bacteria present. 5. Scanning electron microscopy showed that the mutualistic bacterium is not present on major workers immediately following eclosion, indicating that the bacterium is not transferred to callow workers until later. 6. The results of an experiment simulating within-colony transmission to callow workers suggest that the bacterium is predominantly transmitted from older to newly eclosed major workers, but that transmission may also occur via the fungus garden. The presence of Streptomyces bacteria in the fungus garden implies that rare events of horizontal transmission of the fungal cultivar of attine ants may also imply horizontal transmission of strains of the mutualistic bacterium.

Symbiont recognition of mutualistic bacteria by Acromyrmex leaf-cutting ants

“…The ability of ants to recognize their Pseudonocardia strain likely influences these functional aspects of the association. Similarly, recognition likely plays an important role in the maintenance of the ant-bacterium association through the transmission of bacterial inocula from adults to newly emerged workers within colonies (Poulsen et al, 2003b) and by prospective queens between ant generations (Currie et al, 1999b).…”

“…In addition, given that fungusgrowing ants have been shown to exert symbiont choice by behaviorally selecting certain cultivar strains over others (Bot et al, 2001;Mueller et al, 2004), it is also possible that fungus-growing ants can recognize and differentiate between native and nonnative Pseudonocardia strains, allowing active removal of potential competitors of the resident strain. Since the ants incur a significant metabolic cost to support the growth of Pseudonocardia symbiont (Poulsen et al, 2003b;Currie et al, 2006), and the energy consumed by the bacteria for the production of antibiotics against Escovopsis may be diverted to competition when strains mix, maintaining a single Pseudonocardia strain would likely reduce the energetic costs associated with competition, reducing the cost-benefit ratio of the association. At the same time, the ability to distinguish between different Pseudonocardia strains would allow ants to acquire novel strains when confronted with infections by a resistant strain of Escovopsis parasite.…”

Generalized antifungal activity and 454-screening ofPseudonocardiaandAmycolatopsisbacteria in nests of fungus-growing ants

“…Many of the ant-associated Pseudonocardia species show antibiotic activity in vitro against Escovopsis (13)(14)(15). A diversity of actinomycete bacteria including Pseudonocardia also occur in the ant gardens, in the soil surrounding attine nests, and possibly in the substrate used by the ants for fungiculture (16,17).…”

Biological Control Potential of Streptomyces sp. AR10 Producing Albocycline Isolated from Soil around Ant Nest

“…Leaf-cutting ants live in symbiosis with fungi of the genus Leucoagaricus, and the symbiotic fungi serve as a major food source for the ants, and this symbiotic relationship is threatened by another pathogenic fungi. Leaf-cutting ants use actinomycetes to protect the symbiotic fungi from infections by pathogenic fungi (Haeder et al, 2009;Oh, Poulsen, Currie, & Clard, 2009;Poulsen et al, 2003). This symbiotic relationship of leaf cutting ants with actinomycetes are considered to be consistent with the concept of biological control application, and research on biological control using actinomycetes are considered to contribute to sustainable agriculture.…”