The effect of metapleural gland secretion on the growth of a mutualistic bacterium on the cuticle of leaf-cutting ants

Poulsen, Michael; Bot, Adrianne N. M.; Boomsma, Jacobus J.

doi:10.1007/s00114-003-0450-3

Cited by 39 publications

(32 citation statements)

References 16 publications

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“…Increased MG grooming is associated with increased pellet production when ants are challenged with entomopathogenic fungi ( Fernández-Marín et al 2006). This novel behaviour may represent an evolutionary innovation that was necessary because MG secretions, at least in Acromyrmex, inhibit both the ants' fungal symbiont and Pseudonocardia bacteria (Poulsen et al 2003a), which otherwise provide fungus-growing ants with an additional source of antimicrobial compounds (Currie et al 1999b. Much attention has focused on how Pseudonocardia antibiotics control Escovopsis, but our results suggest that Escovopsis is also targeted by MG products, consistent with the demonstration that MG compounds from Acromyrmex reduce germination of Escovopsis .…”

Section: Discussion (A)mentioning

confidence: 95%

Reduced biological control and enhanced chemical pest management in the evolution of fungus farming in ants

et al. 2009

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To combat disease, most fungus-growing ants (Attini) use antibiotics from mutualistic bacteria (Pseudonocardia) that are cultured on the ants' exoskeletons and chemical cocktails from exocrine glands, especially the metapleural glands (MG). Previous work has hypothesized that (i) Pseudonocardia antibiotics are narrow-spectrum and control a fungus (Escovopsis) that parasitizes the ants' fungal symbiont, and (ii) MG secretions have broad-spectrum activity and protect ants and brood. We assessed the relative importance of these lines of defence, and their activity spectra, by scoring abundance of visible Pseudonocardia for nine species from five genera and measuring rates of MG grooming after challenging ants with disease agents of differing virulence. Atta and Sericomyrmex have lost or greatly reduced the abundance of visible bacteria. When challenged with diverse disease agents, including Escovopsis, they significantly increased MG grooming rates and expanded the range of targets. By contrast, species of Acromyrmex and Trachymyrmex maintain abundant Pseudonocardia. When challenged, these species had lower MG grooming rates, targeted primarily to brood. More elaborate MG defences and reduced reliance on mutualistic Pseudonocardia are correlated with larger colony size among attine genera, raising questions about the efficacy of managing disease in large societies with chemical cocktails versus bacterial antimicrobial metabolites.

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Section: Discussion (A)mentioning

confidence: 95%

Reduced biological control and enhanced chemical pest management in the evolution of fungus farming in ants

et al. 2009

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“…Older major workers had previously been proposed as the source of Actinobacterial transmission [39], so we experimentally tested this by exploring the conditions required for major Acromyrmex leaf-cutting ants to acquire natural populations of cuticular Actinobacteria. This confirmed that newly eclosed major workers could acquire exosymbionts in small subcolonies with leaf fragments, fungal garden, and adult majors and minors present.…”

Section: Discussionmentioning

confidence: 99%

Interaction between Workers during a Short Time Window Is Required for Bacterial Symbiont Transmission in Acromyrmex Leaf-Cutting Ants

et al. 2014

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Stable associations between partners over time are critical for the evolution of mutualism. Hosts employ a variety of mechanisms to maintain specificity with bacterial associates. Acromyrmex leaf-cutting ants farm a fungal cultivar as their primary nutrient source. These ants also carry a Pseudonocardia Actinobacteria exosymbiont on their bodies that produces antifungal compounds that help inhibit specialized parasites of the ants' fungal garden. Major workers emerge from their pupal cases (eclose) symbiont-free, but exhibit visible Actinobacterial coverage within 14 days post-eclosion. Using subcolony experiments, we investigate exosymbiont transmission within Acromyrmex colonies. We found successful transmission to newly eclosed major workers fostered by major workers with visible Actinobacteria in all cases (100% acquiring, n = 19). In contrast, newly eclosed major workers reared without exosymbiont-carrying major workers did not acquire visible Actinobacteria (0% acquiring, n = 73). We further show that the majority of ants exposed to major workers with exosymbionts within 2 hours of eclosion acquired bacteria (60.7% acquiring, n = 28), while normal acquisition did not occur when exposure occurred later than 2 hours post-eclosion (0% acquiring, n = 18). Our findings show that transmission of exosymbionts to newly eclosed major workers occurs through interactions with exosymbiont-covered workers within a narrow time window after eclosion. This mode of transmission likely helps ensure the defensive function within colonies, as well as specificity and partner fidelity in the ant-bacterium association.

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“…However, recently emerged workers may be particularly vulnerable to infection as (i) the integument has yet to fully develop its protective layers [18]; (ii) the immune system in younger ants is less active [19]; and (iii) the metapleural glands of young ants might not secrete antibiotics immediately [20]. Thus, extensive symbiotic bacterial bio-films present over the first weeks of adult life could be particularly cost-effective in protecting the most vulnerable colony members.…”

Section: Discussionmentioning

confidence: 99%

Symbiotic bacteria on the cuticle of the leaf-cutting ant Acromyrmex subterraneus subterraneus protect workers from attack by entomopathogenic fungi

2011

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Although only discovered in 1999, the symbiotic filamentous actinobacteria present on the integument of certain species of leaf-cutting ants have been the subject of intense research. These bacteria have been shown to specifically suppress fungal garden parasites by secretion of antibiotics. However, more recently, a wider role for these bacteria has been suggested from research revealing their generalist anti-fungal activity. Here we show, for the first time, evidence for a role of these bacteria in the defence of young worker ants against a fungal entomopathogen. Experimental removal of the bacterial bio-film using an antibiotic resulted in a significant increase in susceptibility of worker ants to infection by the entomopathogenic fungus Metarhizium anisopliae . This is the first direct evidence for the advantage of maintaining a bacterial bio-film on the cuticle as a defensive strategy of the ants themselves and not exclusively for protection of the fungus garden.

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The effect of metapleural gland secretion on the growth of a mutualistic bacterium on the cuticle of leaf-cutting ants

Cited by 39 publications

References 16 publications

Reduced biological control and enhanced chemical pest management in the evolution of fungus farming in ants

Reduced biological control and enhanced chemical pest management in the evolution of fungus farming in ants

Interaction between Workers during a Short Time Window Is Required for Bacterial Symbiont Transmission in Acromyrmex Leaf-Cutting Ants

Symbiotic bacteria on the cuticle of the leaf-cutting ant Acromyrmex subterraneus subterraneus protect workers from attack by entomopathogenic fungi

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