Nutrition mediates the expression of cultivar–farmer conflict in a fungus-growing ant

Abstract

Attine ants evolved farming 55-60 My before humans. Although evolutionarily derived leafcutter ants achieved industrial-scale farming, extant species from basal attine genera continue to farm loosely domesticated fungal cultivars capable of pursuing independent reproductive interests. We used feeding experiments with the basal attine Mycocepurus smithii to test whether reproductive allocation conflicts between farmers and cultivars constrain crop yield, possibly explaining why their mutualism has remained limited in scale and productivity. Stoichiometric and geometric framework approaches showed that carbohydrate-rich substrates maximize growth of both edible hyphae and inedible mushrooms, but that modest protein provisioning can suppress mushroom formation. Worker foraging was consistent with maximizing long-term cultivar performance: ant farmers could neither increase carbohydrate provisioning without cultivars allocating the excess toward mushroom production, nor increase protein provisioning without compromising somatic cultivar growth. Our results confirm that phylogenetically basal attine farming has been very successful over evolutionary time, but that unresolved host-symbiont conflict may have precluded these wildtype symbioses from rising to ecological dominance. That status was achieved by the evolutionarily derived leafcutter ants following full domestication of a coevolving cultivar 30-35 Mya after the first attine ants committed to farming. social evolution | crop domestication | symbiosis | geometric framework | Mycocepurus smithii

The evolution of abdominal microbiomes in fungus‐growing ants

“…After the ancestor of these ants specialized on fungus farming ca. 55–60 MYA, the symbiosis was elaborated in two steps—first by fully domesticating a single lineage of crop fungi which allowed the ants to abandon less specific subsistence farming, and second by developing industrial‐scale leaf‐cutting farming in tighter co‐evolution with increasingly multinucleate and polyploid crop fungi that gradually adapted to decompose more nutritious fresh plant material (De Fine Licht et al, ; Kooij et al, ; Nygaard et al, ; Schultz & Brady, ; Shik et al, ). The attine ant symbiosis with fungus gardens became significantly enriched by cuticular Actinobacteria, which were acquired shortly after the origin of fungus farming and persisted in some, but not all later‐evolving attine genera where their main function appears to be the control of Escovopsis infections or other pathogens in fungus gardens (Barke et al, ; Currie et al, ; Fernandez‐Marin et al, ; Fernández‐Marín, Zimmerman, Nash, Boomsma, & Wcislo, ; Fernández‐Marín, Zimmerman, Rehner, & Wcislo, ; Gerardo et al, ; Haeder et al, ; Mattoso et al, ; Seipke et al, ).…”

The farming ant Sericomyrmex amabilis nutritionally manages its fungal symbiont and its social parasite

“…The shunting of resources to colony growth has been linked to reductions in the fat content of adult workers (Tschinkel, ) and may help explain the reduced %C in S. amabilis workers from parasitised colonies. Second, the nutritional content of fungus gardens probably depends on the nutritional content of foraged substrate (Shik et al ., ). Host ants may thus forage to increase fungus protein content to encourage parasitic consumption of fungal crops rather than host brood.…”

Disentangling nutritional pathways linking leafcutter ants and their co‐evolved fungal symbionts using stable isotopes

“…Leafcutter foragers likely face even greater nutritional challenges as they provision completely unrelated fungal cultivars, saprophytes with very different nutritional requirements (Shik et al. ). And, while we hypothesized that ants would selectively dispose of less desirable crop producing nutrients prior to depositing substrate on the fungus garden, workers actually placed similar amounts of both nutrients directly in their trash piles (Fig.…”

“…Moreover, these diets enabled ants to successfully integrate the nutrients into their farming systems, with ants licking the diets and also cutting pieces and planting them on their gardens (Shik et al. ). Isotopic analyses of 13 C and 15 N (Atom Percent Excess, APE) values, see below ) indicated enrichment for the 1:3 P:C diet of 1.9% 13 C and 6.9% 15 N, and enrichment values for the 3:1 P:C diet of 2.4% 13 C and 4.2% 15 N (see Appendices and : Table S2 for details).…”

“…Since fungal cultivars grow best on specific nutritional blends (Shik et al. ), we tested a waste disposal hypothesis, that a potential mechanism of meeting their cultivar's nutritional needs is that ant farmers select specific nutrients from the composted substrate initially provided to their cultivars through nutrient‐specific disposal of harvested substrates.…”