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Slowing them down will make them lose: a role for attine ant crop fungus in defending pupae against infections?

ABSTRACT: Fungus-growing ants (Attini) have evolved an obligate dependency upon a basidiomycete fungus that they cultivate as their food. Less well known is that the crop fungus is also used by many attine species to cover their eggs, larvae and pupae. The adaptive functional significance of this brood covering is poorly understood. One hypothesis to account for this behaviour is that it is part of the pathogen protection portfolio when many thousands of sister workers live in close proximity and larvae and pupae are not protected by cells, as in bees and wasps, and are immobile. We performed behavioural observations on brood covering in the leaf-cutting ant Acromyrmex echinatior, and we experimentally manipulated mycelial cover on pupae and exposed them to the entomopathogenic fungus Metarhizium brunneum to test for a role in pathogen resistance. Our results show that active mycelial brood covering by workers is a behaviourally plastic trait that varies temporally, and across life stages and castes. The presence of a fungal cover on the pupae reduced the rate at which conidia appeared and the percentage of pupal surface that produced pathogen spores, compared to pupae that had fungal cover experimentally removed or naturally had no mycelial cover. Infected pupae with mycelium had higher survival rates than infected pupae without the cover, although this depended upon the time at which adult sister workers were allowed to interact with pupae. Finally, workers employed higher rates of metapleural gland grooming to infected pupae without mycelium than to infected pupae with mycelium. Our results imply that mycelial brood covering may play a significant role in suppressing the growth and subsequent spread of disease, thus adding a novel layer of protection to their defence portfolio.

SUBMITTER: Armitage SA

PROVIDER: S-EPMC6084299 | biostudies-literature | 2016 Sep

REPOSITORIES: biostudies-literature

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Slowing them down will make them lose: a role for attine ant crop fungus in defending pupae against infections?

Armitage Sophie A O SA Fernández-Marín Hermógenes H Boomsma Jacobus J JJ Wcislo William T WT

The Journal of animal ecology 20160608 5

Fungus-growing ants (Attini) have evolved an obligate dependency upon a basidiomycete fungus that they cultivate as their food. Less well known is that the crop fungus is also used by many attine species to cover their eggs, larvae and pupae. The adaptive functional significance of this brood covering is poorly understood. One hypothesis to account for this behaviour is that it is part of the pathogen protection portfolio when many thousands of sister workers live in close proximity and larvae a ...[more]

PMID: 27136600

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Project description:BackgroundAttine ants live in symbiosis with a basidiomycetous fungus that they rear on a substrate of plant material. This indirect herbivory implies that the symbiosis is likely to be nitrogen deprived, so that specific mechanisms may have evolved to enhance protein availability. We therefore hypothesized that fungal proteinase activity may have been under selection for efficiency and that different classes of proteinases might be involved.ResultsWe determined proteinase activity profiles across a wide pH range for fungus gardens of 14 Panamanian species of fungus-growing ants, representing eight genera. We mapped these activity profiles on an independently obtained molecular phylogeny of the symbionts and show that total proteinase activity in lower attine symbionts peaks at ca. pH 6. The higher attine symbionts that have no known free-living relatives had much higher proteinase activities than the lower attine symbionts. Their total in vitro proteinase activity peaked at pH values around 5, which is close to the pH that the ants maintain in their fungus gardens, suggesting that the pH optimum of fungal proteinases may have changed after the irreversible domestication of evolutionary more derived fungal symbionts. This notion is also supported by buffering capacities of fungus gardens at pH 5.2 being remarkably high, and suggests that the fungal symbiont actively helps to maintain garden acidity at this specific level. Metalloproteinases dominated the activity profiles of lower attine gardens and may thus represent the ancestral type of proteinase production, whereas serine proteinase activity dominated the activity profiles of the higher attine gardens reared by Trachymyrmex and Sericomyrmex, suggesting that there may be trade-offs in the production of these enzyme classes. Remarkably, the single symbiont that is shared by species of the crown group of Atta and Acromyrmex leaf-cutting ants mostly showed metalloproteinase activity, suggesting that recurrent changes in enzyme production may have occurred throughout the domestication history of fungus-garden symbionts.ConclusionsProteinase pH optima and buffering capacities of fungal symbionts appear to have evolved remarkable adaptations to living in obligate symbiosis with farming ants. Although the functional roles of serine and metalloproteinases in fungus gardens are unknown, the differential production of these classes of proteolytic enzymes suggest that substrate specificity may be important and that trade-offs may prevent the simultaneous upregulation of both classes of enzymes.

Dataset Information

Slowing them down will make them lose: a role for attine ant crop fungus in defending pupae against infections?

Publications

Slowing them down will make them lose: a role for attine ant crop fungus in defending pupae against infections?

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