Nutritional niches reveal fundamental domestication trade-offs in fungus-farming ants

Abstract

During crop domestication, human farmers traded greater productivity for higher crop vulnerability outside specialized cultivation conditions. We found a similar domestication tradeoff across the major co-evolutionary transitions in farming systems of attine ants. First, the fundamental nutritional niches (FNNs) of cultivars narrowed during ~ 60 million years of naturally selected domestication, and laboratory experiments showed that ant farmers representing subsequent domestication stages strictly regulate protein harvest relative to cultivar FNNs. Second, ants with different farming systems differed in their abilities to harvest the resources that best matched the nutritional needs of their fungal cultivars. This was assessed by quantifying realized nutritional niches (RNNs) from analyses of items collected from the mandibles of laden ant foragers in the field. Third, extensive field collections suggest that among-colony genetic diversity of cultivars in small-scale farms may offer population-wide resilience benefits that species with large-scale farming colonies achieve by more elaborate and demanding cultivation practices of less diverse crops. Our results underscore that naturally selected farming systems have potential to shed light on nutritional tradeoffs that shaped the course of culturally evolved human farming.

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

“…To assess the effects of minerals on the cultivar performance, we first established a performance baseline by quantifying the cultivar’s FNNs for hyphal growth and staphyla density across an in vitro gradient of protein and carbohydrate (Pr:C) availability. This echoed recent findings (34), but also included lower nutritional concentrations to visualize the cultivar’s FNN across a broader range of plant substrates. Maximal hyphal growth occurred across a broad carbohydrate gradient up to 60% of macronutrient dry mass and with carbohydrate-biased Pr:C ratios ranging from 1:9 to 1:1 Pr:C (i.e.…”

“…Leafcutter ants also face different nutritional challenges than solitary herbivores. First, whereas most herbivores are protein limited (60), leafcutter ants tightly regulate protein intake if given the opportunity because excess protein can cause crop failure (34). Second, regulation of trace minerals is not typically assumed in insect herbivores (4), but fungal cultivars may experience minerals like plant quantitative plant defenses.…”

“…Leafcutter ants have multiple opportunities for such nutritional regulation. First, each type of plant substrate has a specific nutritional profile (Figure 1A), and colonies can target nutritional blends by foraging among leaves, fruits, flowers (32, 33) and across plant species (Figure 1B) (34). Indeed, a single A. colombica colony can forage up to 126 plant species (53 families) and up to 370 kg (dry mass) of plant substrates during an annual cycle (35).…”

“…The next phase occurs when gardener ants within underground fungus cultivation chambers macerate vegetation fragments and add a mixture of enzyme-rich fecal droplets to promote fungal hyphal growth and production of nutrient-rich hyphal tips called gongylidia (packaged in bundles called staphylae) (Figure 1C) (37, 38). Given the potential fungicultural benefits of optimized nutrient provisioning, we conjecture that colonies forage across plant substrates (Figure 1D) to acquire a realized nutritional niche (RNN) that targets cultivar fundamental nutritional niches (FNN) for maximal crop yield (Figure 1E) (34, 39).…”

Proteomics reveals synergy between biomass degrading enzymes and inorganic Fenton chemistry in leaf-cutting ant colonies

“…Neither was there any need initially, because all phylogenetically basal attine ants provision their gardens with dead plant debris. There is a striking difference between the small colonies of these basal attine ants and the large colonies of leaf-cutting ants which are conspicuous functional herbivores with a large ecological footprint (Mehdiabadi and Schultz 2010;Mueller 2002;Shik et al 2020). However, most of the leaves that the ants harvest are heavily protected against herbivory by recalcitrant cell walls and toxic substances (Chen 2008), defences that needed to be overcome for obtaining net nutrition.…”