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

1 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. 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. 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. 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. 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. 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. 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.