The multidimensional nutritional niche of fungus‐cultivar provisioning in free‐ranging colonies of a neotropical leafcutter ant

Crumière, Antonin Jean Johan; James, Aidan; Lannes, Pol; Mallett, Sophie; Michelsen, Anders; Rinnan, Riikka; Shik, Jonathan Z.

doi:10.1111/ele.13865

Cited by 6 publications

(31 citation statements)

References 70 publications

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“…Specifically, we reason that ant pruning severs connections with the main hyphal network and blocks the flow of nutrients to newly isolated fungal cells. Additionally, previous in vitro studies have observed highest staphylae densities at the lowest nutrient concentrations and after a period of days or weeks suggesting that staphyla formation was preceded by a period of nutrient depletion (17,38,71,73,74). Thus, while the focus on cultivar production typically hinges on optimized nutritional provisioning (17,75,76) We next explore the mechanisms by which nuclei may shape the trajectory of gongylidia development through their spatial distributions in hyphal cells.…”

Section: Discussionmentioning

confidence: 99%

“…Additionally, previous in vitro studies have observed highest staphylae densities at the lowest nutrient concentrations and after a period of days or weeks suggesting that staphyla formation was preceded by a period of nutrient depletion (17,38,71,73,74). Thus, while the focus on cultivar production typically hinges on optimized nutritional provisioning (17,75,76) We next explore the mechanisms by which nuclei may shape the trajectory of gongylidia development through their spatial distributions in hyphal cells. As the apical portion a gongylidium bulb develops, it is filled with a single large vacuole, which then obstructs nuclear migration and causes the clustering of nuclei at the bulb-filament interface.…”

Section: Discussionmentioning

confidence: 99%

“…The benefits to ant farmers of being able to regulate the production of edible yield by their crop through their phytochemical provisioning decisions are clear. Yet, these farmers also forage across hundreds of biochemically diverse plant species (59)(60)(61) and the plant fragments they collect contain key nutrients-but these nutrients can occur in suboptimal ratios and concentrations (17). Moreover, plant fragments contain a wealth of recalcitrant compounds (e.g.…”

Section: Discussionmentioning

confidence: 99%

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A domesticated fungal cultivar recycles its cytoplasmic contents as nutritional rewards for its leafcutter ant farmers

Leal-Dutra

Yuen

Guedes

et al. 2022

Preprint

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Leafcutter ants farm a fungal cultivar (Leucoagaricus gongylophorus) that converts inedible vegetation into food that sustains colonies with millions of workers. Like fruits of crops domesticated by humans, L. gongylophorus has evolved specialized nutritional rewards—tiny swollen hyphal cells called gongylidia that package metabolites eaten by ant farmers. Yet, little is known about how gongylidia form, and whether ants regulate this formation through plant-fragment provisioning. We used microscopy and in vitro manipulations to explain the cellular mechanisms governing gongylidium formation. First, L. gongylophorus is polykaryotic (up to 17 haploid nuclei/cell) and our results suggest intracellular nucleus distributions govern gongylidium morphology with their absence in expanding edges arresting apical growth and their presence mediating complex branching patterns. Second, nanoscale TEM imaging shows that the cultivar recycles its own cellular material (e.g. cytosol, mitochondria) through a process called ‘autophagy’ and stores the resulting metabolites in gongylidia. This autophagic pathway is further supported by gongylidium inhibition when isolated fungal cultures are grown on media with autophagy inhibitors (chloroquine, 3-methyladenine). We hypothesize that autophagic nutritional reward production is the ultimate cultivar service and reflects a higher-level organismality adaptation enabled by strict symmetric lifetime commitment between ant farmers and their fungal crop.

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Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

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A domesticated fungal cultivar recycles its cytoplasmic contents as nutritional rewards for its leafcutter ant farmers

Leal-Dutra

Yuen

Guedes

et al. 2022

Preprint

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“…Fresh fungal cultures of L. gongylophorus were isolated from a Panamanian A. colombica colony (Ac-2012-1) onto potato-dextrose agar (PDA) [20]. Isotopically enriched media were prepared by adding 0.1 g l −1 of 13 C-enriched glucose (D-glucose-1-13 C, Sigma-Aldrich, USA) or 0.1 g l −1 of 13 C-enriched cellulose (U- 13 C Cellulose, U-10508, IsoLife, The Netherlands) to PDA.…”

Section: Methods (A) In Vitro Assaysmentioning

confidence: 99%

“…PDA without enriched compounds was the negative control. Inoculation of the fungus followed established protocols with incubation at 23.5°C [ 20 ]. Polycarbonate track-etched (PCTE) membrane discs (diameter 47 mm, PCTE 0.1 µm; GVS, USA) were placed in Petri dishes to facilitate collection of fungal tissues for subsequent analyses after 79 days.…”

Section: Methodsmentioning

confidence: 99%

A fungal symbiont converts provisioned cellulose into edible yield for its leafcutter ant farmers

et al. 2022

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While ants are dominant consumers in terrestrial habitats, only the leafcutters practice herbivory. Leafcutters do this by provisioning a fungal cultivar ( Leucoagaricus gongylophorus ) with freshly cut plant fragments and harnessing its metabolic machinery to convert plant mulch into edible fungal tissue (hyphae and swollen hyphal cells called gongylidia). The cultivar is known to degrade cellulose, but whether it assimilates this ubiquitous but recalcitrant molecule into its nutritional reward structures is unknown. We use in vitro experiments with isotopically labelled cellulose to show that fungal cultures from an Atta colombica leafcutter colony convert cellulose-derived carbon into gongylidia, even when potential bacterial symbionts are excluded. A laboratory feeding experiment showed that cellulose assimilation also occurs in vivo in A. colombica colonies. Analyses of publicly available transcriptomic data further identified a complete, constitutively expressed, cellulose-degradation pathway in the fungal cultivar. Confirming leafcutters use cellulose as a food source sheds light on the eco-evolutionary success of these important herbivores.

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Nutritional challenges of feeding a mutualist: Testing for a nutrient–toxin tradeoff in fungus‐farming leafcutter ants

Crumière

Mallett

Michelsen

et al. 2022

Ecology

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The biochemical heterogeneity of food items often yields tradeoffs as each bite of food tends to contain some nutrients in surplus and others in deficit, as well as other less palatable or even toxic compounds. These multidimensional nutritional challenges are likely to be compounded when foraged foods are used to provision others (e.g., offspring or symbionts) with different physiological needs and tolerances. We explored these challenges in free‐ranging colonies of leafcutter ants that navigate a diverse tropical forest to collect plant fragments they use to provision a co‐evolved fungal cultivar. We tested the prediction that leafcutter farmers face provisioning tradeoffs between the nutritional quality and concentration of toxic tannins in foraged plant fragments. Chemical analyses of plant fragments sampled from the mandibles of Panamanian Atta colombica leafcutter ants provided little support for a nutrient–tannin foraging tradeoff. First, colonies foraged for plant fragments that ranged widely in tannin concentration. Second, high tannin levels did not appear to restrict colonies from selecting plant fragments with blends of protein and carbohydrates that maximized cultivar performance when measured with in vitro experiments. We also tested whether tannins expand the realized nutritional niche selected by leafcutter ants into high‐protein dimensions as: (1) tannins can bind proteins and reduce their accessibility during digestion, and (2) in vitro experiments have shown that excess protein provisioning reduces cultivar performance. Contrary to this hypothesis, the most protein‐rich plant fragments did not have highest tannin levels. More generally, the approach developed here can be used to test how multidimensional interactions between nutrients and toxins shape the costs and benefits of providing care to offspring or symbionts.

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The multidimensional nutritional niche of fungus‐cultivar provisioning in free‐ranging colonies of a neotropical leafcutter ant

Cited by 6 publications

References 70 publications

A domesticated fungal cultivar recycles its cytoplasmic contents as nutritional rewards for its leafcutter ant farmers

A domesticated fungal cultivar recycles its cytoplasmic contents as nutritional rewards for its leafcutter ant farmers

A fungal symbiont converts provisioned cellulose into edible yield for its leafcutter ant farmers

Nutritional challenges of feeding a mutualist: Testing for a nutrient–toxin tradeoff in fungus‐farming leafcutter ants

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